Papaya

22 Papaya Jurandi G. OLIVEIRA, Luis M.M. MORALES, Willian B. SILVA, Aroldo GOMES FILHO and Robert E. PAULL CONTENTS List of Abbreviations............................................................................................................................... 399 22.1 Introduction................................................................................................................................... 399 22.2 Papaya Fruit Development............................................................................................................ 400 22.3 The Physiological Bases of Disorders........................................................................................... 401 22.4 Physiological Disorders in Papaya................................................................................................ 402 22.4.1 Skin Freckles.................................................................................................................... 402 22.4.2 Pulp Flesh Gelling............................................................................................................ 406 22.4.3 Pulp Softening.................................................................................................................. 408 22.4.4 Hard Lumps in Pulp..........................................................................................................410 22.4.5 Chilling Injury...................................................................................................................410 22.4.6 Heat Injury.........................................................................................................................412 22.4.7 Blossom End Defect..........................................................................................................413 22.4.8 Intra-Ovarian Ovaries.......................................................................................................414 22.4.9 Other Disorders.................................................................................................................415 22.5 Conclusion......................................................................................................................................415 References................................................................................................................................................416

List of Abbreviations PD SF ATP PPi HSPs CI MAP HI PHT Max Min

physiological disorders skin freckles adenosine triphosphate pyrophosphate heat shock proteins chilling injury modified atmosphere packaging heat injury postharvest hydrothermal treatment maximum minimum

22.1 Introduction Papaya (Carica papaya L.) is currently produced in approximately 60 countries in the world, spread over almost all the countries of tropical America (South and Central America, and State of Hawaii), India, Thailand, the Philippines, and many other Asian countries, in addition to the Caribbean, tropical Africa, and Australia. The global production of papaya in 2014 was about 12.67 million tons, with India, Brazil, 399

TNF_22_K31725_C022_docbook_indd.indd 399

01-10-2018 22:32:33

400

Postharvest Physiological Disorders in Fruits and Vegetables

Nigeria, Mexico, and Indonesia being the top five producers, responsible for about 80% of global production (FAOSTAT, 2017a). India and Brazil alone produce approximately 60% of world production. The area cultivated with papaya and world production have grown systematically over the last 20 years, with the biggest growth in production, which has translated into increased crop productivity. Papaya is a very important agricultural export product for some developing countries, responsible for $226.75 million from the sale of almost 300,000 tons of fruit in 2013 alone. The international demand for the fruit is highly concentrated, and in the last 20 years, the United States alone has consumed almost 55% of all the fruit commercialized in the world, with Europe, Singapore, Hong Kong, and Canada among the most important destinations for papaya (FAOSTAT, 2017b). Papaya is highly valued around the world because it is a source of nutrients for a healthy diet. The fruit is rich in antioxidants, such as carotenes, vitamin C, and flavonoids; vitamin B complex (folate and pantothenic acid); minerals such as potassium and magnesium; and fiber. Papaya is also used commercially to obtain papain for use in the food industry as a meat softener, as a clearing agent in beer, and in pharmaceutical and cosmetic products (Medina et al., 2003; Oliveira and Vitoria, 2011; Sivakumar and Wall, 2013). Papaya production is limited in many areas due to the incidence of diseases in the field, particularly the papaya ringspot virus, which can ruin the commercial value of entire plantations; extensive postharvest losses due to this virus can range from 30% to 60% of a given harvest (Medina et al., 2003). Among postharvest problems, the occurrence of physiological disorders (PDs) can be an important source of plantation losses. Among the most important PDs today for the cultivation of papayas, we can cite skin freckles (SF), pulp gelling or pulp flesh translucency, pulp softening, hard lumps in pulp, and chilling injury (CI). All of these disorders appear seasonally, with peak moments of occurrence followed by periods with no such incidence, a fact that suggests the influence of weather factors on their occurrence. The objective of this chapter is to provide information regarding the principal physiological disorders that can compromise the production and quality of papaya fruit.

22.2 Papaya Fruit Development Papaya fruit is a berry that can vary widely in both size and shape. Some varieties have fruits weighing less than 100 g, while others can weigh up to 10 kg. Pear-shaped and cylindrical fruits are typical of hermaphrodite plants, while female plants produce rounder fruit. The pericarp is often 2.5 to 3.0 centimeters thick in ripe fruit and is composed of parenchyma cells arranged in three layers with the presence of two sets of five vascular bundles each, one in the dorsal position and the other in the ventral position. A large portion of the fruit volume is due to the internal cavity where the seeds are found (Jiménez et al., 2014). Papaya fruit development can be divided into three phases, based on the principal physiological processes taking place, characterized as growth, ripening, and senescence. These phases describe the different processes taking place during fruit development from its initial formation through the organ’s death. However, many processes are common in the different phases, thereby complicating efforts to clearly distinguish between the end of one phase and the beginning of the next one (Watada et al., 1984). Papayas take an average of 5 months from anthesis to harvest. During warm periods, the papaya growth cycle is shorter, completed in as little as 4 months, while during the cool season, fruit attain physiological maturation in 6 months or more (Berilli et al., 2007). Growth is defined as the development phase in which irreversible increases in the physical attributes of the fruit, such as weight and volume, occur. Maturation is the period leading to physiological maturity once fruit growth and ontogeny have taken place, even when fruit has been removed from the plant, without significant losses in fruit quality with respect to climacteric fruit types, as in the case of papaya (Watada et al., 1984). The final phase of maturation is called ripening, and it is during this period that the most significant fruit development transformations occur, involving changes in color, texture, flavor, and aroma that render fruit palatable for consumption. Seed maturation also takes place during this phase with the change in testa color from white to black (Jain et al., 2003). A large number of physiological, biochemical, and


01-10-2018 22:32:33

Papaya

401

structural changes occur in the pulp during papaya ripening. These include the degradation of the cell wall and the filling in of intercellular spaces with intracellular liquid; changes in the composition of pigments, especially the synthesis of carotenoids; changes in the composition of organic acids; the interconversion of soluble sugars; the synthesis of volatile compounds; and an increase in respiratory activity and ethylene production (Paull et al., 1999; Zhou and Paull, 2001; Wall, 2006; Oliveira and Vitória, 2011; Fabi et al., 2014; Souza et al., 2014; Kelebek et al., 2015). The qualitative and quantitative transformations that occur in papayas during ripening are regulated by changes in hormonal balance and are strongly influenced by genetic factors and environmental conditions. In addition, the changes are largely attributed to the action of ethylene (Fabi et al., 2010; Ming et al., 2012) and to the participation of other phytohormones such as auxins, cytokinins, and gibberellins (McAtee et al., 2013). Once ripening starts, these changes take place very quickly, and papaya reaches peak quality for consumption within 8 to 12 days at a temperature of 25°C (Sivakumar and Wall, 2013). As with other climacteric fruits, the increase in respiration is one of the most notable physiological processes that take place during postharvest ripening. Respiratory rates generally increase two- to fourfold during ripening (Corrêa et al., 2011; Fabi et al., 2010; Souza et al., 2014). However, Paull and Chen (1983) verified an increase of up to nine-fold in the respiratory rate of “Kapoho” papaya during ripening. In spite of this, there are no conclusive data about the relationship between the respiratory patterns of papaya and the ripening process. One reason for this is that papaya respiratory patterns vary greatly and are strongly dependent on the genotype and environmental conditions present during ripening (Paull and Chen, 1983; Bron and Jacomino, 2006; Manenoi and Paull, 2007; Fabi et al., 2010; Souza et al., 2014; Silva et al., 2015a). Respiratory intensity is strongly correlated with pulp softening and changes in the fruit’s skin color (Paull and Chen, 1983; Corrêa et al., 2011; Souza et al., 2014). Lower respiratory intensity is associated with slower fruit ripening (Bron and Jacomino, 2006; Martins et al., 2014). Temperature has the most significant influence on respiratory activity. Waghmare et al. (2014) demonstrated that the respiratory rate increases four- to five-fold when the temperature is increased from 10°C to 30°C. During papaya ripening, the occurrence of peak respiratory activity doesn’t always coincide with the maximum emission of ethylene by the fruit, as various authors have reported (Paull and Chen, 1983; da Silva et al., 2003; Corrêa et al., 2011; Souza et al., 2014). The peak respiration is also reported to take place before or after the ethylene peak (Wills and Widjanarko, 1995; Fabi et al., 2007; Resende et al., 2012), and there are even reports showing more than one respiration peak during the ripening of “Golden” and “Sunrise Solo” papayas (Fonseca et al., 2006). These reports cast doubt on the true significance of respiration peaks with respect to fruit ripening. Similarly, there are questions involving the relationship between ethylene emission and respiration during fruit development. Therefore, if such a relationship exists, and since increases in respiratory activity do not always occur after the increase in ethylene production, ethylene may be coordinating the ripening in the whole fruit, and potential changes may be occurring in fruit tissue ethylene sensitivity (Konishi and Yanagisawa, 2008).

22.3 The Physiological Bases of Disorders PDs due to various causes are common in a wide range of fruit (Lurie et al., 1994; Lurie, 1998), including the papaya (Oliveira et al., 2005; Oliveira and Vitoria, 2011; Azevedo et al., 2015). Disorders result from modification of the normal metabolism or structural integrity of tissue caused by natural endogenous or unfavorable external factors. When a PD-triggering factor is present, natural metabolism can be interrupted, partially repressed, or even accelerated, thereby resulting in alterations with respect to tissue integrity. Symptoms vary greatly depending on the duration and intensity of the occurrence and on the tissue affected. In practical terms, diseases and PDs are frequently mistaken for one another. The main distinguishing factor between these conditions lies in the fact that diseases are necessarily associated with some pathogenic organisms, such as bacteria, fungi, or viruses, while this is not so in the case of PDs. PDs can be divided into two categories: those resulting from internal transformations, such as senescence, and those resulting from adverse external conditions. Senescent tissues are more prone to imbalance in ionic homeostasis and cellular energetics, which can trigger PDs. However, this is not to say


01-10-2018 22:32:33

402

AU: An and Paull 1990 is in the reference list.


that younger tissues are “immune” to PDs. Unripe papaya, for example, is more prone to the “chilling” disorder caused by storage at low temperatures, becoming progressively less susceptible to this disorder as the fruit ripens (An and Paull, 1990; Sivakumar and Wall, 2013). Mitochondria are potential sites for metabolic alterations that lead to PDs. Reactive oxygen species (such as superoxide anion and hydrogen peroxide) in the mitochondria can foster the oxidation of lipids and proteins, particularly when the antioxidant capacity of the tissue is lower than the production of free radicals. The action of free radicals on lipids and proteins drastically affects the integrity of cellular membranes. Loss of cellular compartmentalization capacity influences the ability to transport ions into the cell and accumulate them in the cell and vacuole and to appropriate energy for diverse cellular functions, which affects metabolism in a general way. While some PD symptoms are easily identified, others are much less so. PDs that present few or low levels of symptoms may be overlooked. In some cases, PD symptoms appear before collection of the fruit due to stress conditions originating in the field; in others, symptoms may only be identified after harvest, even though their cause may have begun while the fruit was still attached to the plant. PDs brought about by exposure of the fruit to postharvest stress factors, principally those involving storage under controlled conditions, are also very common. Some factors acting individually favor the development of PDs; others catalyze PD processes in concert with other factors, either simultaneously or sequentially. PD factors can be intrinsic, related to the characteristics of the tissue itself in terms of structural composition, or related to environmental conditions under which the fruit grew or was stored. Among these factors, one can cite the genetic material (species or cultivar); growing practices, especially those related to nutritional content; maturity of the fruit at harvest time; climactic conditions, and storage conditions.

22.4 Physiological Disorders in Papaya Among the most important PDs for papaya today are SF (sometimes called frog skin), pulp flesh translucency, pulp softening, hard lumps in pulp, and CI. In addition, heat injury (HI), blossom end defect, and intra-ovarian ovaries have been reported as PDs with lower rates of incidence for papaya. Some of these PDs appear seasonally, with peak periods during the year followed by periods when the PD does not appear in orchards, a fact demonstrating the influence of climactic factors, especially temperature and rainfall patterns, on the incidence of these PDs.

22.4.1 Skin Freckles

AU: the meaning of “ in nature fruit” is not clear. Please rewrite if possible.

SF is a disorder of abiotic origin (Liberato and Zambolim, 2002; Oliveira et al., 2010; Oliveira and Vitória, 2011) that appears as dark green to brown spots on the fruit’s skin. These spots increase in size and may coalesce to form large circular areas with rough, furrowed tissue on fruit skin, a characteristic causing it to be called frog skin. These blemishes are concentrated on the side of the fruit exposed to direct sunlight (Figure 22.1) and occur at a higher frequency in the middle third of the fruit (Gomes Filho et al., 2006). The spots most commonly appear during the last phase of expansion growth as the fruit approaches full size and following periods of light rain (Reyes and Paull, 1994). The blemishes are visible in both unripe and ripe fruits. SF incidence has had a negative impact for Brazilian papaya producers due to restrictions placed on the exportation of in nature fruit affected by SF and its reduced market value within Brazil. Although it is unassociated with nutritional alterations (Kaiser et al., 1996), this disorder is considered one of the chief obstacles to exportation. The widespread rejection of SF papayas by consumers, therefore, is entirely related to esthetic questions. With the exception of “Golden,” which has a smooth golden skin with little chlorophyll and is less susceptible, most cultivars of the Solo group used in Brazilian orchards have high susceptibility to SF (Oliveira et al., 2005). However, because “Golden” is an unfixed genetic type, the “Golden” cultivar is highly variable (Pinto et al., 2013). This phenotypic variability occurs in skin color and changes to the general appearance of the fruit’s skin as well as in plant size and productivity. It is likely that the recent selections of the most highly productive lines without taking into account questions regarding SF incidence may have left the “Golden” cultivar more susceptible to SF. In any event, currently the Golden


01-10-2018 22:32:33

Papaya

403

FIGURE 22.1 Photos showing symptoms of skin freckles in “Tainung 01” (a) and in “Sunrise Solo” (b) papaya fruit. (a) Photo shows the fruit surface that was directly exposed to the sun, exhibiting the presence of large blemishes. (b) Photo shows numerous small spots, a typical symptom in the papaya “Solo.” (From Jurandi G. Oliveira, North Fluminense State University, Campos dos Goytacazes, Brazil.)

AU: this sentence has been reworded. Please check the meaning.

cultivar presents SF symptoms, depending on cultivation conditions, albeit at a lower frequency than other varieties. While the Formosa group, composed of F1 hybrids such as “Tainung01,” is used extensively by Brazilian papaya growers due to its high productivity, it is nevertheless susceptible to SF, a fact that restricts its export. Although the disorder has been reported in commercial orchards since the 1960s (Ishii and Holtzmann, 1963), its cause has not been fully established. No fungal or bacterial cause has been shown. Climatic factors such as rainfall rates, incidence of radiation, and soil temperature in association with plant characteristics, including transpiration capacity and fruit development stage, are determinant variables in SF occurrence (Reyes and Paull, 1994). In a study of SF incidence carried out in a commercial orchard in the municipality of São Francisco de Itabapoana, RJ, roughly 60 km from the city of Campos dos Goytacazes, RJ, peak SF occurrence was from September to November (Figure 22.2), a period with higher temperature amplitude (Table 22.1). The most consistent hypotheses regarding the causes of SF take into account the content and turgor of the latex in skin lactifers (Reyes and Paull, 1994; Kaiser et al., 1996; Oliveira et al., 2010; Oliveira and Vitória, 2011). The causal factors leading to increased lactiferous pressure, which could help explain SF occurrence, include excess water in soil or very high daily temperature amplitudes, as well as high air humidity (Downton, 1981; Reyes and Paull, 1994; Campostrini et al., 2005; Gomes Filho et al., 2007, 2008; Reis et al., 2008). Some reports have implicated intrinsic factors related to fruit and skin tissue, such as latex vessel density and the wall structure of lactiferous cells, as well as fruit calcium levels and soluble solids levels of the latex, that increase the predisposition of fruit toward SF formation (Da Cunha et al., 1998; Campostrini et al., 2005; Reis et al., 2008; Reyes and Paull, 1994). All such intrinsically genetic


AU: If this is a citation, no matching reference was found. Search WorldCat

01-10-2018 22:32:34

404


FIGURE 22.2 Standard symptoms for skin freckles in cv. Tainung 01 papaya samples in a commercial orchard in the city of São Francisco de Itabapoana, Rio de Janeiro, Brazil, from 2000 to 2001. Numbers represent estimates of blemish incidence in the fruit areas sampled. Each grid sample represents an area of 6.25 mm2. (From Oliveira, J.G., and Vitória, A.P., Food Res. Int., 44, 1306, 2011.)

TABLE 22.1 Maximum (Max) and Minimum (Min) Temperature and Temperature Amplitude (T. ampl.) from October 2000 to September 2001 in a Commercial Orchard in the São Francisco de Itabapoana, RJ (21°28′25″ S, 41°7′13″ W). Data Represent the Average for the Month

Max (°C) Min (°C) T. ampl. (°C)

AU: this sentence has been reworded. Please check the meaning.

Jan

Feb

Mar

Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

29.7 22.5 7.2

30.8 22.4 8.4

30.0 21.8 8.2

29.3 21.3 8.0

28.4 20.0 8.4

27.1 17.6 9.5

25.9 17.5 8.4

27.3 17.8 9.5

28.8 17.9 10.9

29.3 20.2 9.1

29.3 21.4 7.8

31.3 22.8 8.5

factors may modulate internal lactiferous pressure and consequently encourage or inhibit SF occurrence, thus explaining the presence of genetically differing levels of susceptibility to the disorder (Oliveira et al., 2005). Attempts have been made to avoid SF occurrence in the field through the application of carnauba wax and kaolinite (rock powder) and by wrapping fruit in sheets of aluminum-layered polyethylene 30 days prior to harvest (Figures 22.3 and 22.4). The application of coating and wrapping fruit are not regarded as cost-effective. In addition, wrapping fruit increases the humidity at the fruit surfaces and the incidence of black spot disease (Asperisporium caricae [Speg.] Maubl.) on the fruit. Nevertheless, the use of aluminum-layered sheeting disproved the hypothesis that SF was caused by wind-blown solids such as sand grains. Wrapped fruits had less SF than the unwrapped fruit, but wrapping was not completely effective in preventing SF occurrence (Figure 22.4). These results support the hypothesis that the origin of the disorder is most likely related to an internal process beginning within the fruit; leakage from latex vessels into the surrounding skin tissue spreads into the external tissue, resulting in blemishes on the fruit skin. Striving to minimize peak variations in the turgor pressure of lactiferous vessels, Gomes Filho et al. (2007, 2008) studied different irrigation practices and soil covering materials in an effort to restrict the


01-10-2018 22:32:35

Papaya

405

FIGURE 22.3 Papaya fruit wrapped in aluminum-layered polyethylene in an orchard in São Francisco de Itabapoana, RJ. The SF-free fruit were wrapped approximately 30 days before their harvest date. (From Oliveira, J.G., and Vitória, A.P., Food Res. Int., 44, 1306, 2011.)

FIGURE 22.4 SF incidence in wrapped and unwrapped papaya fruits. Wrapped fruits remained on the plants, and approximately 10 fruits per plant were removed per sampling. Fruit evaluation took place about 30 days after the beginning of treatment. Grid numbers are estimates of SF fruit within sample areas. Each grid represents an area of 6.25 mm 2.

disorder in Golden and Tainung 01, but these treatments were not effective to decrease the occurrence of SF in papaya. A viable alternative is the development of genetically improved materials bearing higher tolerance to the PD. Such efforts require public and private initiatives to elucidate the causal factors related to this disorder, which is related to high losses in productivity for Brazilian growers. Growers in several countries have employed SF-resistant materials. The Sekati cultivar, known as “Hong Kong Papaya,” for example, has been used extensively in Malaysia and has fared well in the Asian market. This cultivar performed well for SF resistance when compared with the Tainung 01 hybrid (Yamanishi et al., 2006). Researchers have sought to identify genetic materials that are less susceptible to SF, working chiefly to introduce materials of the Formosa group. Genetic materials with high potential for use as sources of increased SF resistance are being used in the Papaya Plant Breeding Program of the Universidade Estadual do Norte Fluminense in Campos dos Goytacazes (RJ), Brazil (Oliveira et al.,


01-10-2018 22:32:36

406


2005; Pinto et al., 2013). It is highly likely that in the near future, papaya producers will be making use of this material.

22.4.2 Pulp Flesh Gelling The disorder known as “pulp flesh gelling,” “pulp gelling,” or “pulp flesh translucency” causes serious damage to papaya fruit quality, representing a problem for papaya growers in some Brazilian production areas where incidence of the disorder is high. Because affected fruit do not exhibit external symptoms, identification of the disorder rarely occurs in the field. Pulp gelling is often only discovered on opening the fruit, thus creating serious problems for papaya marketing. The disorder is most prevalent in the winter months (Oliveira et al., 2010; Oliveira and Vitoria, 2011). The disorder receives its name from the darkening of the pulp hue and a jelly-like or “soaked” texture (Oliveira and Vitória, 2011). Symptoms develop from the endocarp toward the exocarp without ever revealing external signs of the process (Figure 22.5). As the disorder develops, fruit become denser as large quantities of water accumulate in the seed cavity, and the fruit tend to sink in packinghouse fruit washing tanks. In the first reports of the occurrence of this disorder in a plantation in the Brazilian municipality of Linhares (ES), pulp gelling was compared to the “internal pulp collapse” disorder, common in mangoes, due to their slight visual similarity. However, closer examination revealed that the two processes bear distinct differences in terms of both cause and symptoms (Oliveira et al., 2010). One characteristic feature of affected fruit is the separation of the flesh from the skin, especially in the part of the fruit where the gelling symptom is most pronounced (Figure 22.6). In such cases, it is possible to “unpeel” the papaya pulp from the skin as if peeling a banana. The literature contains limited information with respect to the occurrence of pulp gelling in papayas. At present, the disorder has only been confirmed in the growing areas of Espírito Santo State in southeastern Brazil in cv. Golden papaya. Unconfirmed reports have also claimed that gelling has occurred in cv. Sunrise fruit in southern Bahia State orchards in the northeastern region of Brazil. The condition has parallels to the appearance of over-ripened fruit in other varieties. In Hawaii, similar symptoms occur occasionally in fruit that are still green. As previously stated, observation of the disorder suggests that large quantities of water in the intercellular spaces results in soaking of the mesocarp tissue (Oliveira et al., 2010; Oliveira and Vitoria, 2011). Surface analysis of cuts by scanning electron microscopy have revealed that in healthy papaya, pulp tissue is intact, containing normal intercellular spaces (Figure 22.7a). In gelled pulp, however, plasmolyzed cells appear, containing large spaces between them (Figure 22.7b, see arrow).

AU: is Vitória or Vitoria the correct spelling?

AU: no arrow is visible in Figure 22.7b.

FIGURE 22.5 Golden papaya fruit with internal symptoms of pulp flesh translucency, showing a healthy (left) and flesh translucency (right) fruit (a). Outer appearance of the fruit with no symptoms to distinguish it from healthy fruit (left) and from those with flesh translucency (right) (b). (From Oliveira, J.G., and Vitória, A.P., Food Res. Int., 44, 1306, 2011.)


01-10-2018 22:32:37

Papaya

407

FIGURE 22.6 Golden papaya fruit with pulp flesh translucency symptoms. It is possible to observe that the skin of the fruit detaches easily from the pulp, a condition not typically found in healthy fruits. (From Oliveira, J.G., and Vitória, A.P., Food Res. Int., 44, 1306, 2011.)

FIGURE 22.7 Samples of healthy (a, c, and e) and flesh translucency (b, d, and f) papaya fruit mesocarp. Scanning electron micrographs (a and b) show plasmolyzed cells and intercellular spaces in pulp flesh translucency (arrows), bars = 100 μm. Light microscopy (c and d) shows the intercellular space in pulp flesh translucency (arrow), bars = 20 μm. Transmission electron microscopy from cell wall (e and f) showing disestablished cell wall in pulp flesh translucency, bars = 0.5 μm. (From Oliveira, J.G. et al., Rev. Bras. Frutic., 32, 961, 2010.)


AU: arrows are not visible in Figure 22.7.

01-10-2018 22:32:38

408


The physical state of the mesocarp of gelled fruit could be confused with an abnormal ripening process, since this would result in a loosening of the mesocarp tissue. However, the plasmolyzed cells, as well as the pulp firmness (Oliveira et al., 2010), do not support the idea of precocious tissue ripening. The comparison of samples of healthy and pulp gelled fruit in an optical microscope confirmed increased spacing between the cells of gelled mesocarp (Figures 22.7c and 22.7d). Transmission electron microscope analysis did not reveal degeneration of the cell wall. The image did suggest, however, lower cell wall rigidity in fruit presenting pulp gelling symptoms (Figure 22.7f) when compared with healthy fruit (Figure 22.7e). Results currently indicate that the gelled appearance of the pulp of “Golden” papaya fruit is not related to premature ripening of the fruit, nor is it directly related to a calcium deficiency in the fruit. The data suggest that the inhibition of water entering into the vacuole and, consequently, the loss of cellular turgor lead to a PD, and that the soaked appearance of the tissue is due to the accumulation of water in the apoplast (Azevedo et al., 2015). According to Azevedo et al. (2015), the cause of the gelled papaya tissue is a dysfunction in its capacity to accumulate intercellular water related to the activity of both V-type tonoplast (EC 3.6.1.34) and P-type plasma membrane (EC 3.6.1.35) H+-transporting ATPase. These proton pumps play a central role in the function of the cell membranes by generating and maintaining an electrochemical gradient that energizes the secondary transport of many ions, such as Mg2+, K+, and Ca2+, and also of sugars, organic acids, and other metabolites (Zeng et al., 2012; Etienne et al., 2013). In addition, an H+-transporting inorganic pyrophosphatase (V-PPase; EC 3.6.1.1), present in the tonoplast, constitutes the proton pump system in plant cells. These enzymes are able to couple the chemical energy of ATP hydrolysis or of pyrophosphate (PPi) to the translocation of cytoplasm protons outside the cell or from the cytoplasm into the vacuole. In their analysis of the functioning of the pumps present in the plasma membrane, Azevedo et al. (2015) found a reduction in the availability of energy for the transport of ions and other solutes, such as sucrose, to the cytoplasm, which partially explains the lower K+ concentration and total soluble solids in the pulp tissue of gelled fruits (Oliveira et al., 2010). According to Azevedo et al. (2015), gelled tissue membranes have a very high permeability rate, and this leakiness meant that the tonoplast was unable to maintain the cellular turgor pressure of the gelled tissue. This data is consistent with the anatomical features of fruit with plasmolyzed cells. In addition, Azevedo et al. (2015) speculate that some hormonal (such as auxin) imbalance could be involved in the elicitation of the V-ATPase uncoupling as well as a possible reversible inactivation of V-ATPase triggered by low temperatures (Matsuura-Endo et al., 1992). The latter is consistent with early reports of the greater occurrence of the gelling disorder in papaya plantations during the colder period of the year (Oliveira et al., 2010; Oliveira and Vitoria, 2011). The gelling of pulp can be easily confused with internal pulp collapse, a PD that occurs in mangoes. In internal collapse in mango, the determining factor for the disorder is a calcium deficiency (Hojo et al., 2009). Ca2+ is often related to the occurrence of PDs and changes in fruit texture (Bangerth, 1979; Ferguson et al., 1999; Sams, 1999; Silva et al., 2015b). During the initial phase, the visual symptoms of internal collapse in mangoes are somewhat similar to those of papaya pulp gelling. Due to the similarity, some have hypothesized that these two disorders stem from the same causes or may indeed be the same disorder. However, the results obtained by Oliveira et al. (2010) show that calcium level and pulp firmness in fruit with gelling do not differ (P < .05) in relation to healthy ones. Therefore, the results lead to the conclusion that papaya pulp gelling is unrelated to both internal collapse in mangoes and calcium deficiency.

22.4.3 Pulp Softening Standard softening of papaya pulp occurs 6 to 12 days after the harvesting of green, ripe fruit (known as color break). Internally, the fruit pulp shows changes in the mesocarp color that extend from the region close to the seed cavity toward the skin. During this process, the pulp color changes from a slightly greenish white to an orange-yellow, salmon, or reddish color, depending on the variety, and significant textural alterations take place with the pulp becoming softer (Wall, 2006). Ripe papaya pulp chiefly consists of parenchyma cells with a large volume of thin cell walls that are not highly resistant to compression or physical impact (Oliveira and Vitoria, 2011).


01-10-2018 22:32:38

Papaya

409

FIGURE 22.8 Pulp softening in papaya. Note that the fruit shows an excessive softening of the whole fruit even in the green-ripe (3/4 ripe) stage. (Source: Chay-Prove, P., Papaw Information Kit (series: Agrilink Series: your guide to better farming), The State of Queensland, Department of Primary Industries, 2000. With permission.)

While it is true that fruit ripening can be confused with the PD of pulp softening, papayas exhibiting this disorder generally lose firmness over the entire fruit (Figure 22.8). This softening may take place prematurely in green-ripe fruit (¼ to ½ ripe) or through the excessive softening of fully ripe fruit. Environmental factors and orchard management (i.e., irrigation and mineral nutrition), as well as physiological and genetic factors, are the principal components influencing fruit texture. Loss of tissue texture occurs due to water loss through tissue transpiration or as a consequence of developmental processes involving sequences of genetically programmed biochemical events during the ripening phase. Loss of water from papaya fruit occurs through the cut stem and fruit skin. Loss through the skin increases after the 50% ripe stage as the fruit cuticle is disrupted by latex (Paull and Chen, 1989). Water loss is a minor cause of texture loss when compared with cell wall changes that take place during fruit ripening. Structural modification occurring in the cell wall resulting in pulp softening can be observed by histological analyses (Pereira et al., 2009; Fabi et al., 2014). These modifications are related to transformations in the principal constituents of the cell wall, including cellulose, hemicellulose, pectic substances, and structural proteins (Paull and Chen, 1983; Manenoi and Paull, 2007; Thumdee et al., 2010), subjected to the action of enzymes regulated by genes expressed during papaya ripening (Paull et al., 2008; Fabi et al., 2014). Light intensity, water availability in the soil, and especially the temperatures at which fruit develop are among the most important environmental factors affecting fruit texture. Light is required for fruit development and can improve fruit texture, but high light and intense exposure can increase fruit temperature and may result in loss of firmness and sunburn (Sams, 1999). There is a correlation between fruit temperature and firmness, especially in sunburnt fruit. Fruit have a higher firmness when they develop with more moderate temperatures. This response pattern stems from a reduction in the size of fruit cells that grew at low temperatures, resulting in a denser tissue with a higher percentage of cell wall in relation to cell volume. Smaller fruit generally have firmer consistency than larger ones, and to a certain extent, this observation can be extended to comparisons between fruit of the Solo and Formosa groups. The provision of excess nitrogen in the field can result in a loss of fruit firmness (Sams, 1999). However, this alteration in texture resulting from high doses of N is due to the indirect action of N (in excess) on mesocarp tissue’s capacity to accumulate calcium (Qiu et al., 1995). During fruit ripening, loss of pulp firmness is preceded by Ca loss from its binding sites on the cell wall structure and middle lamella (Qiu et al., 1995). Potassium is not directly related to papaya fruit texture. This element does play a significant role in the tissue’s turgor potential (Qiu et al., 1995). Because this disorder increases the susceptibility of fruits to mechanical damage, it is of extreme importance in terms of the postharvest fruit management. The successful handling of fruit, from harvest to packinghouse and especially during the transport of papayas to markets, is seriously compromised when fruits do not possess the necessary structural integrity to withstand the compression and mechanical impacts that commonly occur. This issue is of even greater relevance when fruit are transported in bulk, a practice that continues to be used extensively by small commercial establishments in poorer growing regions and in markets supplying low-income consumers, despite recommendations against its


01-10-2018 22:32:39

410


use. Mechanical damage is a problem when handling fruit from both the Solo and Formosa groups. This damage is more prevalent in the internal markets of developing countries such as Brazil, Mexico, SouthEast Asia and India, although it is also considered to be one of the principal postharvest problems for papayas sent from Hawaii to the U.S. mainland (Paull et al., 1997; Oliveira and Vitoria, 2011).

22.4.4 Hard Lumps in Pulp

AU: does “ The disorder was barely verified” mean that there was very little incidence of the disorder?

The disorder known as hard lumps has been described in papayas by some authors (Paull and Chen, 1990; Paull, 1995), and its occurrence has been associated with weather conditions, specifically high temperatures (Paull, 1995; Oliveira and Vitoria, 2011). This disorder is characterized by the formation of highly distinct areas of the mesocarp in which tissue is firmer than in the surrounding areas (Figure 22.9). Fruit do not exhibit external symptoms that would differentiate them from unaffected fruit, leading to a downgrading of the fruit’s commercial value that may affect the whole shipment. The occurrence of this disorder has not been well studied with respect to the genetic material grown in Brazil or the different climactic conditions. Few studies have investigated the natural occurrence of hard fruit in orchards throughout the year to identify periods with higher incidence. The inability to predict its occurrence and its sporadic occurrence and the inability to create the condition on harvested fruit make research difficult. Some unquantified statements have reported the occurrence of this disorder in summer, especially during January and February, the period of highest temperatures in Brazil. The reports are from orchards located in the municipality of Pureza (state of Rio Grande do Norte), an important Brazilian papaya-growing region supplying the European market (regional producers, personal communication). According to these reports, the fruit harvested at ripening stages I and II (yellowing up to 25% of surface area) were affected by hard lumps during the fruit’s ripening phase. The disorder was barely verified in fruit from the Golden variety during the summer months (December to March), whereas it did not appear during the rest of the year. For growing conditions in Hawaii, United States, Paull (1995) found that fruit sensitivity to hard lumps increased during the winter months and was highly correlated with the postharvest hydrothermal treatment performed for fruit fly larval disinfestation and to control disease. Hard lumps in pulp are probably the result of the inactivation of cell wall degrading enzymes due to high-temperature stress, which also inhibits the emission of ethylene and alters skin and pulp coloration in papayas (Paull, 1995). Thermotolerance can be induced artificially (Paull and Chen, 1990) or result from natural inducing conditions in the growing environment (i.e., preharvest climactic conditions, especially temperature (Paull, 1995; Ferguson et al., 1999). The synthesis of heat shock proteins (HSPs) does occur in papaya following heat stress and impart thermal tolerance.

22.4.5 Chilling Injury CI is a disorder generally observed in fruit of tropical and subtropical origin in which plant tissues exposed to low temperatures acquire physiological injury (Almeida et al., 2005). In general, the most

FIGURE 22.9 Papaya fruit with symptoms of hard lumps in pulp. In the fruit on the right, it is possible to observe clearly a distinct region with firmer pulp. (From Robert E. Paull, University of Hawaii, Honolulu, United States.)


01-10-2018 22:32:39

Papaya

411

FIGURE 22.10 Chilling injury in papaya fruit. (a) Image showing an external view of the fruit with green areas surrounding a pitted area of the skin. The fruit shows a blotchy appearance. (From Chay-Prove, P., Papaw Information Kit (series: Agrilink Series: your guide to better farming), The State of Queensland, Department of Primary Industries, 2000. With permission.) (b) Cut fruit showing the internal CI with dark areas that do not soften during the ripening of the fruit pulp. (From Jurandi G. Oliveira, North Fluminense State University, Campos dos Goytacazes, Brazil.)

AU: An and Paull is in the reference list.

common symptoms of CI on fruit are skin scald, hard lumps in the pulp around the vascular bundles, uneven ripening, inferior fruit flavor and carotenoids content, water soaking of flesh, and increased susceptibility to postharvest pathogens (Figure 22.10) (Thompson and Lee, 1971; El-Tomi et al., 1974; Chen and Paull, 1986; Chay-Prove, 2000; Rivera-Pastrana et al., 2010; Bautista-Baños et al., 2013; Sivakumar and Wall, 2013). Stress from cold temperatures causes various changes in cellular activity, including changes in membrane structure that affect permeability, which can lead to leakage of electrolytes or even oxidative stress (Lyons, 1973; Graham and Patterson, 1982; Shadmani et al., 2015). Under chilling stress, fruit initially exhibit an increase in tissue respiration followed by a decrease in respiratory rate or even respiratory decoupling related to phosphorylation and energy production difficulties (Graham and Patterson, 1982; An and Paull, 1990). Furthermore, ethylene production has been associated with CI of papaya fruit (Sivakumar and Wall, 2013; Zou et al., 2014). In fact, changes in the expression levels of genes involved both in the synthesis and in the signal transduction of ethylene have been verified (Zou et al., 2014). However, the role of ethylene in the development of chilling stress in papaya fruit is not fully elucidated. Papaya shelf life is therefore influenced by fruit storage temperatures. This disorder arises when fruit are stored at temperatures below the critical limit or when the time of storage exceeds standard practice limits. The temperatures that induce CI differ among fruit species, and fruit skin is generally more susceptible to injury than the pulp (Mitra, 1997). Storing papaya at low temperature is a common practice in the fruit handling and marketing chain, especially when it is necessary to postpone ripening to transport fruit to consumer markets far from the growing regions. The control of chilling stress is to store fruit above the critical limit (Chen and Paull, 1986; Paull, 1999; Sivakumar and Wall, 2013). Storage temperature recommendations for papaya vary between 7 and 13°C, depending on the papaya variety, fruit ripening stage, and storage time (Chen and Paull, 1986; Cámara et al., 1993; Proulx et al., 2005; Rocha et al., 2005; Rivera-Pastrana et al., 2010; Sivakumar and Wall, 2013; Gomes et al., 2016). Fruit becomes progressively less susceptible to chilling stress as it ripens (Chen and Paull, 1986). Ripe, full-color fruit can be held for more than a week at 1 to 3°C. Papaya fruit at color-turning (break) stage can be stored at 7°C for 14 days and will ripen normally when transferred to room temperature (Chen and Paull, 1986). Gomes et al. (2016) report that “Golden” papayas stored for 10 days at a temperature of 10°C did not develop chilling symptoms. Preconditioning treatments at higher temperatures can help minimize or eliminate CI during storage. Pérez-Carrillo and Yahia (2004) pretreated “Maradol” papaya at 48.5°C for 4 minutes before storing fruit at 5°C and reported a lower incidence of CI. Similarly, Ali et al. (2000) reported that treating “Eksotika” papaya at a temperature of 38°C for 6 to 24 hours before transfer to low-temperature storage reduced chilling stress. According to Huajaikaew et al. (2005), before storing fruits at 5°C, the preconditioning of “Sunrise” papaya at 45°C for 6 hours increased tolerance to chilling stress. The use of alternating temperatures for 17 days (two periods of fruit storage at 20°C within the 5-day


01-10-2018 22:32:40

412



chilled storage cycle) did not increase internal injury but increased chilling-related skin scald (Chen and Paull, 1986). Although calcium has been shown to induce susceptibility to CI in mature green papaya (Chen and Paull, 1986), studies have shown its effects on other fruits to be the opposite; that is, calcium could prevent CI in fruits (Wang, 1982; Tsantili et al., 2002; Jiao et al., 2017). According to Chen and Paull (1986), chilling-induced skin scald and internal injury had positive linear correlations with the treatment of papaya fruit at 0%, 1%, and 5% (w/v) concentrations of CaCl2. The calcium in plants apparently strengthens cell walls and cell membranes and helps tissues withstand chilling stress (Wang, 1982). In addition, Chen and Paull (1986) demonstrated that preconditioning treatments such as waxing and wrapping papaya with polyethylene were effective in reducing CI. UV-C irradiation reduced susceptibility to CI in “Maradol” (Rivera-Pastrana et al., 2014). CI symptoms also were diminished in “Sunrise” papaya with methyl jasmonate (10 −4 M) treatment and modified atmosphere packaging (MAP) under cold storage (Gonzalez-Aguilar et al., 2003). These strategies for the reduction of CI through the use of high temperature, UV-C irradiation, jasmonate, ethylene absorbers, and MAP involve different protective mechanisms against CI. For example, heat-induced chilling tolerance has been associated with more resistant cellular membranes, increased antioxidant enzyme activity, and lower lipid peroxidation (Huajaikaew et al., 2005; Zhang et al., 2005). The decrease of CI by UV-C irradiation was due to activation of the defense mechanisms of the plant, including an increase in flavonoid synthesis in skin and enhanced catalase activity in fruit pulp (RiveraPastrana et al., 2014). The inhibition of CI by low O2 and high CO2 concentrations may be related to reduced water loss and altered ethylene biosynthesis and sensitivity (Zagory and Kader, 1988). Methyl jasmonate was reported to reduce CI via a mechanism that involves an increase in abscisic acid and polyamine levels (Wang and Buta, 1999).

22.4.6 Heat Injury HI is due to variation in the sensitivity of fruit to thermal treatment during the year and preharvest and postharvest conditions (Paull, 1995; Paull et al., 1997; Lurie, 1998; Corrêa et al., 2008). The most common symptoms that occur as a consequence of heat treatments are external, that is, darkening or discoloration of the skin and accelerated senescence, as well as internal, that is, failure of fruit to soften fully or softening at a reduced rate, water loss, and darkening of pulp coloration (Lurie, 1998; Pimentel et al., 2007). In the “Golden” papaya, failure of pulp to soften during ripening due to heat stress results in a firmer than normal product, as happens in the case of the “hard lumps in pulp” disorder (Oliveira and Vitoria, 2011). During HI, there are clearly marked areas on the mesocarp in which the tissue is much firmer than in the neighboring areas without any external symptoms that would distinguish it from unaffected fruits (Oliveira and Vitoria, 2011). Sometimes, the symptoms of HI can be confused with CI (Figure 22.11). According to Paull and Chen (2000), the influence of heat on postharvest fruit ripening is dependent on (i) the level of field-induced thermotolerance, (ii) the cultivar, (iii) fruit size and morphological characteristics, (iv) physiological state (stage of ripeness), (v) heat transfer rate and energy balance (thermal difference, heat capacity, and relative humidity), (vi) final temperature, and (vii) the duration of exposure to different temperatures. Also, fruit color influences the preharvest thermal history of a fruit. Surface temperatures of dark green fruit may reach 24°C above ambient air temperatures, while light-colored fruit may only be 10–12°C above ambient. The extent of HI in fruit is a function of exposure temperature and duration and how quickly the fruit is cooled following the heat treatment (Paull et al., 1997; Lurie, 1998; Pimentel et al., 2007; Fan et al., 2011). Correa et al. (2012) demonstrated that different postharvest hydrothermal treatments (PHT) reduced firmness while increasing the emission of metabolic gases in ripening “Golden” papaya, showing the high sensitivity of papaya pulp to heat stress. In terms of cellular functions, HI involves protein denaturation, disruption of protein synthesis, alteration of the skin color, climacteric respiration, ethylene production, and loss of membrane integrity (Lurie, 1998; Paull and Chen, 2000; Oliveira and Vitoria, 2011). Protein denaturation at lethal temperatures is regarded as non-reversible, while at lower temperatures, reversible inactivation may still be possible.


01-10-2018 22:32:40

Papaya

413

FIGURE 22.11 Papaya fruit with symptom of heat injury. It is possible to observe area on the pulp fruit closer to the seeds cavity with tissue much firmer (pulp color lighter) than in the neighboring area. (From Jurandi G. Oliveira, North Fluminense State University, Campos dos Goytacazes, Brazil.)


Attempts to increase the tolerance of fruit to thermal stress have been empirically developed to reduce the injury caused by heat treatment. These strategies include the use of preconditioning procedures, just as in the case of inducing tolerance to chilling stress. Studies with papaya fruit have demonstrated that exposure to elevated, sub-lethal temperatures induces thermotolerance, which protects fruit from a second exposure to a normally higher temperature. In papaya, often the heat treatment consists of 20-minute immersion in water (or vapor heat or hot forced air) at 48 ± 1°C (Paull and Chen, 1990, 2000; Pimentel et al., 2007; Corrêa et al., 2008), a procedure that can frequently cause HI. Paull and Chen et al. (1990) verified that papaya fruit softening by injurious heat treatment was reduced or prevented with a pretreatment at 42°C for 1 hour, or by varying the pretreatment time to 38°C, with both treatments followed by a 3-hour rest at 22°C. While the development of thermotolerance is dependent on exposure temperature and has been associated with the synthesis of HSP, loss of thermotolerance has been associated with the disappearance of HSP (Lurie, 1998; Oliveira and Vitoria, 2011). HSPs produced in response to high temperatures are believed to prevent irreversible protein denaturation, which would be detrimental to the cell (Lurie, 1998), and this activity may be enhanced in plants by small HSPs (Lee and Vierling, 2000). To induce thermotolerance, the exposure temperature must be high enough to initiate the synthesis of HSP, but not so hot that transcription and translation of HSP are inhibited. HSPs are produced within 30 min after exposure to moderate temperatures. Temperatures of 35–40°C have been found to be effective, depending on the fruit (Paull and Chen, 1990, 2000; Lurie, 1998; Woolf and Ferguson, 2000). At 42°C or higher, HSP synthesis is attenuated, and fruits are more likely to suffer heat damage (Ferguson et al., 1994). As decay of HSPs occurs, there is a corresponding loss in thermotolerance. High preharvest temperatures in the orchard may naturally promote a tolerance response in fruit that undergo high temperatures postharvest, thereby reducing HI. Reports by Paull (1995) corroborate this hypothesis. This author showed that when the average temperature of the three days before harvest was between 17 and 31°C, there was a significant correlation with an increase in the resistance of papaya fruit to damage caused by exposure to temperatures of 49°C (standard disinfestation treatment: 48 ± 1°C for 20 min). On the other hand, preharvest factors related to plantation management (such as calcium availability) may encourage the incidence of HI in papayas. Paull (1995) found that fruit with high calcium levels in the mesocarp were sensitive to heat and more susceptible to HI, despite reports of Ca2+-related thermotolerance in plants (Bokszczanin and Fragkostefanakis, 2013).

AU: please check and correct “ Paull and Chen et al.”

22.4.7 Blossom End Defect According to Liquido (1990), while there are several ways a defective blossom end may become apparent, an opening (with a diameter of >7 mm) that extends all the way to the seed cavity of the fruit generally occurs. The disorder leaves an open channel at the blossom end of the fruit cavity (Figure 22.12). This disorder is caused by a developmental failure of placental growth to close the stigmal canal during early


01-10-2018 22:32:40

414


FIGURE 22.12 Blossom end defect in papaya fruit. Images showing an external visible opening (a) and in the fruit cut longitudinally an open channel at the blossom end of the fruit cavity (b). (From Chay-Prove, P., Papaw Information Kit (series: Agrilink Series: your guide to better farming), The State of Queensland, Department of Primary Industries, 2000. With permission.)

fruit growth (Paull et al., 1997), when the carpels at the style end of the ovary occasionally fail to fuse completely (Zee and Nishina, 1989). Liquido (1990) proposes three categories for blossom end defects: small pinhole (hole ~1 mm in diameter), large pinhole (hole >1 mm in diameter), and navel (resembling the blossom end of a navel orange). The author found that the correlation between fruit infested with fruit fly eggs and the size of the opening of the blossom end defect was not significant. Zee and Nishina (1989) state that the “Kapoho” papaya is more prone to blossom end defect disorder than the “Sunrise” variety due to the latter’s more elliptical fruit shape with better carpel fusion. Fruit with this disorder are generally prone to bacterial diseases in the fruit seed cavity before normal harvest. Fruits with a defective blossom end generally ripen earlier, but in some cases need to be culled, because the pulp presents strong fetid odors due to bacterial growth. Some researchers suspected that this natural “opening” in the fruit may foster oviposition by flies (Zee and Nishina, 1989), but according to Liquido (1990), the percentage infestation rate by the oriental fruit fly (Dacus dorsalis Hendel) in normal “Kapoho Solo” fruit and in those with blossom end defect was the same for mature green to colorbreak fruits. According to this author, this is due to the oriental fruit fly’s and the melon fly’s standard practice of depositing eggs on fruit surface areas other than the blossom end. The blossom end defect is a disorder of low incidence in the field and appears seasonally (Zee and Nishina, 1989; Paull et al., 1997), suggesting the influence of climatic factors on its occurrence. Perhaps due to the low occurrence rate of this disorder in the field, the literature contains few studies on it.

22.4.8 Intra-Ovarian Ovaries “Intra-ovarian ovaries,” or “intra-ovarian fruits,” is an unusually interesting teratological phenomenon described in papaya (Bergman, 1921; Nakasone and Arkle, 1971; Paull et al., 1997). The fruit containing intra-ovarian ovaries show no external symptoms, which complicate the disorder’s identification. The earliest report on this disorder (Bergman, 1921) describes the presence of five small secondary fruit within the seed cavity of papaya. These were attached near the basal end of the fruit, growing out from the placenta and replacing the seeds (Figure 22.13). According to Bergman (1921), four of the five secondary fruit consisted of an ovary surmounted by a sessile stigma that was not completely developed; in any case, only a single carpel was probably represented. Each of the four larger enclosed fruit possessed a few regular seeds, even containing an embryo of normal shape and size. The secondary fruit were yellowish and slightly paler than the normal fruit. A microscopic examination of the epidermis of these fruit, performed by Bergman (1921), revealed that it was composed of cells similar in shape to, but somewhat larger than, epidermal cells of normal fruit. Although this similarity extended even to the presence of stomata, the guard cells did not contain chloroplasts. The cross-section of the structure of the enclosed fruit resembled that of normal fruit except for the absence of wax coating and the presence


01-10-2018 22:32:41

Papaya

415

FIGURE 22.13 Cut papaya fruit showing the presence of secondary fruit within the seed cavity of fruit. (a) (From Bergman, H.F., Botanical Gazette, 72, 97, 1921.) (b) (From http://imgur.com/a/qboj5.)

of a thinner epidermis. For Bergman (1921), this disorder does not originate from the metamorphosed ovules that occur on the placentae. According to this author, intra-ovarial fruit probably arise from buds that develop adventitiously in places normally occupied by ovules. There is very little information available in the literature about this disorder. The report by Paull et al. (1997) on “intra-ovarian ovaries” describes this disorder as a proliferation of tissue in the seed cavity, which can form a thread-like appendage with round or elongated structures of various sizes and shapes, a few of which fill the entire seed cavity of the fruit and have their own cavity with non-viable seeds. This description differs from that reported by Bergman (1921), which showed the proliferation of “small secondary fruits” with seeds inside the seed cavity of the fruit.

22.4.9 Other Disorders There are other papaya orchard disorders of very low incidence cited in the literature, including i) “sun scald,” occurring in fruit that develop on trees with very sparse foliage and/or on trees that are leaning over, when the fruit are directly exposed to the sun, and where picked fruit is left exposed to the sun (Paull et al., 1997); ii) “sunken dry brownish areas” resulting from the feeding of mites on fruit skin during early growth. According to Paull et al. (1997), this disorder is generally caused by the red and black mite (Brevipalpus phoenicis [Geijskes]) in Hawaii; and iii) carpelloid fruit (also called cat-faced), is an abnormal, commercially worthless fruit generated due to the fusion of stamen of hermaphrodite flowers with the ovary that occurs during early flower development (Figure 22.14). This disorder is associated with genetic and environmental factors; low temperature is a promoter of the disorder, while its genetic nature needs to be understood (Martelleto et al., 2011).

22.5 Conclusion The physiological disorders discussed in this chapter commonly occur in many of the world’s principal papaya-growing regions. Because such disorders are potentially harmful to the quality of fruits, they warrant investment in research and study related to their occurrence. These studies should involve three courses of action, which could all be performed by individual teams or research groups or by distinct groups working in diverse locations that share access to new results. These courses of action are:

1. The first step should be to perform surveys to generate and organize precise data, using reproducible methods, to improve knowledge regarding the patterns of occurrence for each disorder throughout the plant cycle. Such studies should monitor climatic variables (temperature, precipitation, relative humidity, sun hours, etc.), which are fundamental data for interpreting variations in the incidence of disorders. While this is not always possible, research activities would ideally be reproduced consecutively over years or in different locations to gauge the maximum number of variables related to the interaction between the environment and plant physiological


01-10-2018 22:32:42

416


FIGURE 22.14 Carpelloid fruit. Note that it is possible to see at least two carpelloid fruit among the normal fruit on a papaya tree. (From Robert E. Paull, University of Hawaii, Honolulu, United States.)

states. These efforts should promote participation and collaboration between growers and eyewitnesses, for this could result in greater efficiency with respect to time and financial expense. 2. Both during and after completion of the surveys, research efforts should be directed at understanding the physiological, biochemical, and molecular mechanisms involved in the occurrence of disorders. Comprehension of this information is often quite difficult to achieve due to the fact that it frequently involves the untangling of causes from their effects. The integration of research and human resources from related scientific areas (phytotechnology, plant physiology, chemistry, physics, plant breeding, molecular biology, etc.) can offer a powerful tool for the resolution of this conundrum. Once one is in possession of a model describing the triggering mechanism for a disorder being studied, the next step (when possible) would be to promote and simulate the situations and scenarios thought to induce it. 3. In the field, plantation management should be modified to apply treatments and conditions found to have potential to induce a given disorder and not merely those that may inhibit it. It is important to remember that in the field, uncontrolled factors may be highly unpredictable. For this reason, field studies should be conducted in more than one location. The assessment of disorder incidence rates under modified growing conditions, as well as the selection of less susceptible genotypes, is an important step before performing the formal analysis of results, which should undergo statistical evaluation. 4. Finally, information generated in the field related to the relative susceptibility of available genotypes and the mechanisms affecting the incidence of PDs in fruit should be incorporated into plant breeding programs and made available to producers to improve the selection of genotypes for use in the environmental conditions at hand, thereby minimizing the occurrence of fruit disorders in the field.

REFERENCES Ali, Z.M., Ng, C.H., Chua, S.T., Othman, R., and Lazan, H. 2000. Heat treatment alleviates chilling injury symptoms, retards texture changes and maintains the capacity to produce ethylene in papaya fruits. pp. 519–524. In: F. Artcs, M.I. Gil and M.A. Conesa (eds.). Improving Postharvest Technologies of Fruits, Vegetables and Ornamentals. International Institute of Refrigeration, Paris. Almeida, R.F., Resende, E.D., Vitorazi, L., Carlos, L.A., Pinto, L.K.A., Silva, H.R.F., and Martins, M.L.L. 2005. Chilling injury in papaya fruits (Carica papaya L.) cv “Golden.” Revista Brasileira de Fruticultura 27, 17–20. An, J.F., and Paull, R.E. 1990. Storage temperature and ethylene influence on ripening of papaya fruit. Journal of the American Society for Horticultural Science 115, 949–953.


01-10-2018 22:32:43

Papaya

417

Azevedo, I., Façanha, A., Olivares, F., and Oliveira, J.G. 2015. Functional uncoupling of the tonoplast proton pump and its effect on the flesh gelling physiological disorder in papaya fruit. Scientia Horticulturae 187, 115–121. Bangerth, F. 1979. Calcium-related physiological disorders of plants. Annual Review of Phytopathology 17, 97–122. Bautista-Baños, S., Sivakumar, D., Bello-Pérez, A., Villanueva-Arce, R., and Hernández-López, M. 2013. A review of the management alternatives for controlling fungi on papaya fruit during the postharvest supply chain. Crop Protection 49, 8–20. Bergman, H.F. 1921. Intra-ovarial fruits in Carica papaya. Botanical Gazette 72, 97–101. Berilli, S.S., Oliveira, J.G., Marinho, A.B., Lyra, G.B., Souza, E.F., Viana, A.P., Bernardo, S., and Pereira, M.G. 2007. Avaliação da taxa de crescimento de frutos de mamão (Carica papaya L.) em função das épocas do ano e graus-dias acumulados. Revista Brasileira de Fruticultura 29, 11–14. Bokszczanin, K.L., Solanaceae Pollen Thermotolerance Initial Training Network (SPOT-ITN) Consortium, and Fragkostefanakis, S. 2013. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Frontiers in Plant Science 4, 315. Bron, I.U., and Jacomino, A.P. 2006. Ripening and quality of “golden” papaya fruit harvested at different maturity stages. Brazilian Journal of Plant Physiology 18, 389–396. Cámara, M.M., Diez, C., and Torija, M.E. 1993. Changes during ripening of papaya fruit in different storage systems. Food Chemistry 46, 81–84. Campostrini, E., Lima, H.C., Oliveira, J.G., Monnerat, P.H., and Marinho, C.S. 2005. Teores de Ca e variáveis meteorológicas: Relação com a incidência da mancha fisiológica do mamão do Norte Fluminense. Bragantia 64, 601–613. Chay-Prove, P.M. 2000. Papaw Information Kit. Agrilink Series: Your Growing Guide to Better Farming. Queensland Horticulture Institute, Department of Primary Industries, Brisbane, Queensland. Chen, N.M., and Paull, R.E. 1986. Development and prevention of chilling injury in papaya fruit. Journal of the American Society for Horticultural Science 111, 639–643. Corrêa, S.F., da Silva, M.G., Pereira, T., Almeida Jr., P.S.G., Vargas, H., Oliveira, J.G., and Berilli, S.S. 2012. Influence of hydrothermal treatments on papaya fruit (Carica papaya L.). Acta Horticulturae 934, 695–701. Corrêa, S.F., de Souza, M.S., Pereira, T., de Lima Alves, G., de Oliveira, J.G., da Silva, M.G., and Vargas, H. 2008. Determination of thermal diffusivity in papaya pulp as a function of maturation stage. Revista Brasileira de Fruticultura 30, 611–615. Corrêa, S.F., Mota, L., Paiva, L.B., Couto, F.M., Silva, M.G., Oliveira, J.G., Sthel, M.S., Vargas, H., and Miklós, A. 2011. Effects of ozone exposure on “golden” papaya fruit by photoacoustic phase-resolved method: Physiological changes associated with carbon dioxide and ethylene emission rates during ripening. Journal of Applied Physics 109, 114701. Da Cunha, M., Costa, C.G., Machado, R.D., and Miguens, F.C. 1998. Distribution and differentiation of the laticifer system in Chamaesyce thymifolia (L.) Millsp. (Euphorbiaceae). Acta Botanica 47, 209–218. da Silva, M.G., Santos, E.O., Sthel, M.S., Cardoso, S.L., Cavalli, A., Monteiro, A.R., de Oliveira, J.G., Pereira, M.G., and Vargas, H. 2003. Effect of heat treatment on ethylene and CO2 emissions rates during papaya (Carica papaya L.) fruit ripening. Review of Scientific Instruments 74, 703–705. Downton, W.J.S. 1981. Water relations of laticifers in Nerium oleander. Australian Journal of Plant Physiology 8, 329–334. Eloisa, M., Reyes, Q., and Paull, R.E. 1994. Skin freckles on solo papaya fruit. Scientia Horticulturae 58, 31–39. El-Tomi, A.L., Abon-Aziz, A.B., Abdel-Kader, A.S., and Abdel-Wahab, F.K. 1974. The effect of chilling and non-chilling temperatures on the quality of papaya fruit. Egyptian Journal of Horticulture 1, 179–185. Etienne, A., Genard, M., Lobit, P., Mbeguié-A-Mbéguié, D., and Bugaud, C. 2013. What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. Journal of Experimental Botany 64, 1451–1469. Fabi, J.P., Broetto, S.G., da Silva, S.L., Zhong, S., Lajolo, F.M., and do Nascimento, J.R. 2014. Analysis of papaya cell wall-related genes during fruit ripening indicates a central role of polygalacturonases during pulp softening. PLOS ONE 9. Fabi, J.P., Cordenunsi, B.R., de Mattos Barreto, G.P., Mercadante, A.Z., Lajolo, F.M., and Oliveira do Nascimento, J.R. 2007. Papaya fruit ripening: Response to ethylene and 1-methylcyclopropene (1-MCP). Journal of Agricultural and Food Chemistry 55, 6118–6123.


01-10-2018 22:32:43

418


Fabi, J.P., Mendes, L.R.B.C., Lajolo, F.M., and Nascimento, J.R.O. 2010. Transcript profiling of papaya fruit reveals differentially expressed genes associated with fruit ripening. Plant Science 179, 225–233. Fan, L., Song, J., Forney, C.F., and Jordan, M.A. 2011. Fruit maturity affects the response of apples to heat stress. Postharvest Biology and Technology 62, 35–42. FAOSTAT 2017a. Crop production. www.fao.org/faostat/en/#data/QC (accessed March 20, 2018). FAOSTAT 2017b. Crops and livestock products. www.fao.org/faostat/en/#data/TP (accessed March 20, 2018). Ferguson, I., Volz, R., and Woolf, A. 1999. Preharvest factors affecting physiological disorders of fruit. Postharvest Biology and Technology 15, 255–262. Ferguson, I.B., Lurie, S., and Bowen, J.H. 1994. Protein synthesis and breakdown during heat shock of cultured pear (Pyrus communis L.) cells. Plant Physiology 104, 1429–1437. Fonseca, M.J.O., Leal, N.R., Cenci, S.A., Cecon, P.R., Bressan-Smith, R.E., and Balbino, J.M.S. 2006. Evolução dos pigmentos durante o amadurecimento de mamão “Sunrise Solo” e “Golden.” Revista Brasileira de Fruticultura 29, 451–455. Gomes, B.L., Fabi, J.P., and Purgatto, E. 2016. Cold storage affects the volatile profile and expression of a putative linalool synthase of papaya fruit. Food Research International 89, 654–660. Gomes Filho, A., de Oliveira, J.G., Viana, A.P., Damasceno Júnior, P.C., and Pereira, M.G. 2006. Validação do método das notas para quantificação da incidência da mancha fisiológica do mamão através do uso de imagens digitais. Revista Brasileira de Fruticultura 28, 365–368. Gomes Filho, A., de Oliveira, J.G., Viana, A.P., and Pereira, M.G. 2007. Lâminas de irrigação e coberturas de solo sobre a incidência da mancha fisiológica e produtividade do mamão “golden.” Ciência Rural 37, 1654–1660. Gomes Filho, A., de Oliveira, J.G., Viana, A.P., and Pereira, M.G. 2008. Mancha fisiológica e produtividade do mamão Tainung 01: Efeito da lâmina de irrigação e cobertura do solo. Ciência e Agrotecnologia 32, 1161–1167. Gonzalez-Aguilar, G.A., Buta, J.G., and Wang, C.Y. 2003. Methyl jasmonate and modified atmosphere packaging (MAP) reduce decay and maintain postharvest quality of papaya “Sunrise.” Postharvest Biology and Technology 28, 361–370. Graham, D., and Patterson, B.D. 1982. Responses of plants to low, nonfreezing temperatures: Proteins, metabolism, and acclimation. Annual Review of Plant Physiology 33, 347–372. Hojo, R.H., São José, A.R., Hojo, E.T.D., Alves, J.F.T., Rebouças, T.N.H., and Dias, N.O. 2009. Qualidade de manga “Tommy Atkins” pós-colheita com uso de cloreto de cálcio na pré-colheita. Revista Brasileira de Fruticultura 31, 62–70. Huajaikaew, L., Uthairatanakij, A., Kanlayanarat, S., and Gemma, H. 2005. Effect of heat treatment on antioxidants in papaya fruit stored at low temperature. Acta Horticulturae 682, 1063–1068. Ishii, M., and Holtzmann, O.V. 1963. Papaya mosaic disease in Hawaii. Plant Disease Reporter 47, 951–970. Jain, N., Dhawan, K., Malhotra, S., and Singh, R. 2003. Biochemistry of fruit ripening of guava (Psidium guajava L.): Compositional and enzymatic changes. Plant Foods for Human Nutrition 58, 309–315. Jiao, W., Xi, Y., Cao, J., Fan, X., and Jiang, W. 2017. Regulatory effects of CaCl2, sodium isoascorbate, and 1-methylcyclopropene on chilling injury of banana fruit at two ripening stages and the mechanisms involved. Journal of Food Processing and Preservation 42, e13442. Jiménez, V.M., Mora-Newcomer, E., and Gutiérrez-Soto, M.V. 2014. Biology of the papaya plant. pp. 17–33. In: R. Ming and P.H. Moore (eds.), Genetics and Genomics of Papaya, Plant Genetics and Genomics: Crops and Models 10. Springer, New York. Kaiser, C., Allan, P., White, B.J., and Dehrmann, F.M. 1996. Some morphological and physiological aspects of freckle on papaya (Carica papaya L.) fruit. Journal of the Southern African Society of Horticultural Science 6, 37–40. Kelebek, H., Selli, S., Gubbuk, H., and Gunes, E. 2015. Comparative evaluation of volatiles, phenolics, sugars, organic acids and antioxidant properties of Sel-42 and Tainung papaya varieties. Food Chemistry 173, 912–919. Konishi, M., and Yanagisawa, S. 2008. Two different mechanisms control ethylene sensitivity in Arabidopsis via the regulation of EBF2 expression. Plant Signaling & Behavior 3, 749–751. Lee, G.J., and Vierling, E. 2000. A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiology 122, 189–198. Liberato, J.R., and Zambolim, L. 2002. Controle das doenças causadas por fungos, bactérias e nematóides em mamoeiro. pp. 1023–1170. In: L. Zambolim, F.X.R. do Vale, A.J.A. Monteiro and H. Costa (eds.). Controle de Doenças de Plantas Fruteiras. Editora UFV, Viçosa.


01-10-2018 22:32:43

Papaya

419

Liquido, N.J. 1990. Morphological defects in the blossom end of papaya fruits in relation to infestation rates by oriental fruit fly and melon fly (Diptera: Tephritidae). Journal of Economic Entomology 83, 1883–1887. Lurie, S. 1998. Postharvest heat treatments. Postharvest Biology and Technology 14, 257–269. Lurie, S., Klein, J.D., and Fallik, E. 1994. Cross protection of one stress by another: Strategies in postharvest fruit storage. pp. 201–212. In: J.H. Cherry (ed.). Biochemical and Cellular Mechanisms of Stress Tolerance in Plants: Series H. Cell Biology 86. Springer, Berlin. Lyons, J.M. 1973. Chilling injury in plants. Annual Review of Plant Physiology 24, 445–466. Manenoi, A., and Paull, R.E. 2007. Papaya fruit softening, endoxylanase gene expression, protein and activity. Physiologia Plantarum 131, 470–480. Martelleto, L.A.P., Ribeiro, R.L.D., Sudo-Martelleto, M., Vasconcellos, M.A.S., and Pereira, M.B. 2011. Expression of female sterility and carpelloidy on papaya tree under different environments of protected cultivation. Revista Brasileira de Fruticultura 33, 1185-1193. Martins, D.R., Barbosa, N.C., and de Resende, E.D. 2014. Respiration rate of golden papaya stored under refrigeration and with different controlled atmospheres. Scientia Agricola 71, 369–373. Matsuura-Endo, C., Maeshima, M., and Yoshida, S. 1992. Mechanism of the decline in vacuolar H+-ATPase from mung bean hypocotyls during chilling. Plant Physiology 100, 718–722. McAtee, P., Karim, S., Schaffer, R.J., and David, K. 2013. A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening. Frontiers in Plant Science 4, 79. Medina, J.C., Gutiérrez, G.V., and García, H.S. 2003. PAWPAW (Papaya): Post-harvest Operation. AGST, FAO. Ming, R., Yu, Q., Moore, P.H., Paull, R.E., Chen, N.J., Wang, M.-L., Zhu, Y.J., et al. 2012. Genome of papaya, a fast growing tropical fruit tree. Tree Genetics & Genomes 8, 445–462. Mitra, S.K. 1997. Postharvest Physiology and Storage of Tropical and Subtropical Fruits. CABI Publishing, New York. Nakasone, H.Y., and Arkle, T.D. 1971. Development of intra-ovarian ovaries in Carica papaya L. Journal of the American Society for Horticultural Science 96, 550–553. Oliveira, J.G., and Vitória, A.P. 2011. Papaya: Nutritional and pharmacological characterization, and quality loss due to physiological disorders. An overview. Food Research International 44, 1306–1313. Oliveira, J.G., Bressan-Smith, R.E., Campostrini, E., Da Cinha, M., Costa, E.S., Netto, A.T., Coutinho, K.S., Silva, M.G., and Vitória, A.P. 2010. Papaya pulp gelling: is it premature ripening or problems of water accumulation in the apoplast? Revista Brasileira de Fruticultura 32, 961-969. Oliveira, J.G., Pereira, M.G., Martelleto, L.A.R., and Ide, C.D. 2005. Skin freckle on papaya fruit. A perspective of obtaining tolerant genotypes. Revista Brasileira de Fruticultura 27, 458–461. Paull, R.E. 1995. Preharvest factors and the heat sensitivity of field-grown ripening papaya fruit. Postharvest Biology and Technology 6, 167–175. Paull, R.E. 1999. Effect of temperature and relative humidity on fresh commodity quality. Postharvest Biology and Technology 15, 263–277. Paull, R.E., and Chen, N.J. 1983. Postharvest variation in cell wall-degrading enzymes of papaya (Carica papaya L.) during fruit ripening. Plant Physiology 72, 382–385. Paull, R.E., and Chen, N.J. 1989. Waxing and plastic wraps influence water loss from papaya fruit during storage and ripening. Journal of the American Society for Horticultural Science 114, 937–942. Paull, R.E., and Chen, N.J. 1990. Heat shock response in field-grown, ripening papaya fruit. Journal of the American Society for Horticultural Science 115, 623–631. Paull, R.E., and Chen, N.J. 2000. Heat treatment and fruit ripening. Postharvest Biology and Technology 21, 21–37. Paull, R.E., Gross, K., and Qiu, Y. 1999. Changes in papaya cell walls during fruit ripening. Postharvest Biology and Technology 16, 79–89. Paull, R.E., Irikura, B., Wu, P., Turano, H., Chen, N.J., and Blas, A. 2008. Fruit development, ripening and quality related genes in the papaya genome. Tropical Plant Biology 1, 246-277. Paull, R.E., Nishijima, W., Reyes, M., and Cavaletto, C. 1997. Postharvest handling and losses during marketing of papaya (Carica papaya L.). Postharvest Biology and Technology 11, 165–179. Pereira, T., de Almeida, P.S.G., de Azevedo, I.G., da Cunha, M., de Oliveira, J.G., da Silva, M.G., and Vargas, H. 2009. Gas diffusion in “golden” papaya fruit at different maturity stages. Postharvest Biology and Technology 54, 123–130.


01-10-2018 22:32:43

420

AU: This was matched as Spanish, but the detected title language is Portuguese. Is this spelled correctly?


Pérez-Carrillo, E., and Yahia, E.M. 2004. Effect of postharvest hot air and fungicide treatments on the quality of “Maradol” papaya (Carica papaya L.). Journal of Food Quality 27, 127–139. Pimentel, R.M., Marcondes, Y.E.M., and Walder, J.M.M. 2007. Qualidade do mamão cv. Solo submetido ao choque térmico e tratamento quarentenário por radiação gama. Revista Brasileira de Fruticultura 29, 483–487. Pinto, F. de Oliveira, Ramos, H.C.C., Cardoso, D.L., da Luz, L.N., and Pereira, M.G. 2013. Development of papaya genotypes (Carica papaya L.) tolerant to skin freckles. Revista Brasileira de Fruticultura 35, 1101–1115. Proulx, E., Nunes, M.C.N., Emond, J.P., and Brecht, J.K. 2005. Quality attributes limiting papaya postharvest life at chilling and non-chilling temperatures. Proceedings of the Florida State Horticultural Society 118, 389–395. Qiu, Y., Nishina, M.S., and Paull, R.E. 1995. Papaya fruit growth, calcium uptake, and fruit ripening. Journal of the American Society for Horticultural Science 120, 246–253. Reis, F.O., Campostrini, E., and Netto, A.T. 2008. Mancha fisiológica do mamão “Formosa”: Relações com o potencial hídrico do solo, o teor de sólidos solúveis totais do látex e as variáveis do clima. Ciência e Agrotecnologia 3, 1473–1480. Resende, E.C.O., Martins, P.F., Azevedo, R.A., Jacomino, A.P., and Bron, I.U. 2012. Oxidative processes during “Golden” papaya fruit ripening. Brazilian Journal of Plant Physiology 24, 85–94. Rivera-Pastrana, D.M., Gardea, A.A., Yahia, E.M., Martínez-Téllez, M.A., and González-Aguilar, G.A. 2014. Effect of UV-C irradiation and low temperature storage on bioactive compounds, antioxidant enzymes and radical scavenging activity of papaya fruit. Journal of Food Science and Technology 51, 3821–3829. Rivera-Pastrana, D.M., Yahia, E.M., and González-Aguilar, G.A. 2010. Phenolic and carotenoid profiles of papaya (Carica papaya L.) and their contents under low temperature storage. Journal of the Science of Food and Agriculture 90, 2358–2365. Rocha, R.H.C., de Carvalho Nascimento, S.R., Menezes, J.B., de Sousa Nunes, G.HS., and Silva, E.O. 2005. Qualidade pós-colheita do mamão formosa armazenado sob refrigeração. Revista Brasileira de Fruticultura 27, 386–389. Sams, C.E. 1999. Preharvest factors affecting postharvest texture. Postharvest Biology and Technology 15, 249–254. Shadmani, N., Ahmad, S.H., Saari, N., Ding, P., and Tajidin, N.E. 2015. Chilling injury incidence and antioxidant enzyme activities of Carica papaya L. “Frangi” as influenced by postharvest hot water treatment and storage temperature. Postharvest Biology and Technology 99, 114–119. Silva, L.R.A., Silva, G.M.C., Silva, W.B., Souza, C.L.M., and Oliveira, J.G. 2015a. Respiratory activity in isolated mitochondria from pulp of UENF/CALIMAN01 and Tainung01 papaya in postharvest fruit conservation. Revista Brasileira de Fruticultura 37, 296–307. Silva, W.B., Silva, G.M.C., Silva, L.R.A., Waldman, W.R., and Oliveira, J.G. 2015b. Treatment with calcium chloride at postharvest delays the degreening and loss of firmness of papaya UENF/Caliman01. Revista Brasileira de Fruticultura 37, 588–599. Sivakumar, D., and Wall, M.M. 2013. Papaya fruit quality management during the postharvest supply chain. Food Reviews International 29, 24–48. Souza, A.F., Silva, W.B., Gonçalves, Y.S., Silva, M.G., and Oliveira, J.G. 2014. Ripening physiology of varieties of papaya commercialized in Brazil. Revista Brasileira de Fruticultura 36, 318–328. Thompson, A.K., and Lee, G.R. 1971. Factors affecting the storage behaviour of papaya fruit. Journal of Horticultural Science 46, 511–516. Thumdee, S., Manenoi, A., Chen, N.J., and Paull, R.E. 2010. Papaya fruit softening: role of hydrolases. Tropical Plant Biology 3, 98–109. Tsantili, E., Konstantinidis, K., Athanasopoulos, P.E., and Pontikis, C. 2002. Effects of postharvest calcium treatments on respiration and quality attributes in lemon fruit during storage. The Journal of Horticultural Science and Biotechnology 77, 479–484. Waghmare, R.B., Mahajan, P.V., and Annapure, U.S. 2014. Modelling the influence of time and temperature on respiration rate of fresh fig and diced papaya. International Journal of Food Engineering 10, 89–96. Wall, M.M. 2006. Ascorbic acid, vitamin A, and mineral composition of banana (Musa sp.) and papaya (Carica papaya) cultivars grown in Hawaii. Journal of Food Composition and Analysis 19, 434–445. Wang, C.Y. 1982. Physiological and biochemical responses of plants to chilling stress. Hortscience 17, 173–186.


01-10-2018 22:32:43

Papaya

421

Wang, C.Y., and Buta, J.G. 1999. Methyl jasmonate improves quality of stored zucchini squash. Journal of Food Quality 22, 663–670. Watada, A.E., Herner, R.C., Kader, A.A., Romani, R.J., and Staby, G.L. 1984. Terminology for the description of developmental stages of horticultural crops. HortScience 19, 20–21. Wills, R.B.H., and Widjanarko, S.B. 1995. Changes in physiology, composition and sensory characteristics of Australian papaya during ripening. Australian Journal of Experimental Agriculture 35, 1173–1176. Woolf, A.B., and Ferguson, I.B. 2000. Postharvest responses to high fruit temperatures in the field. Postharvest Biology and Technology 21, 7–20. Yamanishi, O.K., Mello, R.M., Martins, V.A., Lima, L.A., and Fagundes, G.R. 2006. Comportamento do mamoeiro “Sekati” nas condições do oeste da Bahia. Revista Brasileira de Fruticultura 28, 79–82. Zagory, D., and Kader, A.A. 1988. Modified atmosphere packaging of fresh produce. Food Technology 42, 70–77. Zee, F.T., Nishina, M.S., Chan Jr, H.T., and Nishijima, K.A. 1989. Blossom end defects and fruit fly infestation in papayas following hot water quarantine treatment. HortScience 24, 323–325. Zeng, H., Liu, G., Kinoshita, T., Zhang, R., Zhu, Y., Shen, Q., and Xu, G. 2012. Stimulation of phosphorus uptake by ammonium nutrition involves plasma membrane H+-ATPase in rice roots. Plant and Soil 357, 205–214. Zhou, L., and Paull, R.E. 2001. Sucrose metabolism during papaya (Carica papaya) fruit growth and ripening. Journal of the American Society for Horticultural Science 126, 351–357. Zou, Y., Zhang, L., Rao, S., Zhu, X., Ye, L., Chen, W., and Li, X. 2014. The relationship between the expression of ethylene-related genes and papaya fruit ripening disorder caused by chilling injury. PLOS ONE 9.


01-10-2018 22:32:43


01-10-2018 22:32:43