Photosynthetic Response and Adaptation to

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ANNUAL REVIEWS Ann. Rev. Plant Physiol 198a 31:491-543 Copyright © /98() by Annual Reviews Inc. All rights reserved

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PHOTOSYNTHETIC RESPONSE

.7699

AND ADAPTATION TO TEMPERATURE IN HIGHER PLANTS Joseph Berry and Olle Bjorkman 1

Department of Plant Biology, Carnegie Institution of Washington, Stanford, California 94305

CONTENTS INTRODUCTION ECOLOGICAL ASPECTS OF PHOTOSYNTHETIC TEMPERATURE ADAPTATION ............................................................................................ Photosynthetic Temperature Dependence in Thermally Contrasting Climates .. Photosynthetic Temperature Acclimation . . .. Seasonal acclimation in natural habitats . . ........................................... Studies in controlled environments .. . . . . . .. . ... . THE MECHANISTIC BASIS FOR PHOTOSYNTHETIC RESPONSE AND ADAPTATION TO TEMPERATURE .................................................... Reversible Temperature Respon.ses . . .. .. . . . . . . . Stomata! effec� o� the temJH!.rature response 0/photo.rynthesis .................................... . Interacttons with /lght mtenslty . . . . . . . .. . . .. . . C, photo.rynthesis (lM photorespiration . . .......................................................... C, photo.rynthesis .................................................................................................... Comparison 0/plants from contrasting thermol regimes . . . ...................... ["eversible Temperature Respon.ses . . .. . . Low temperature sensitMty ............................................................................... High temperature sensitivity . .. .. . .. . .... ... ... ..... ........ . .. .... .... .... .... .. Adoptive responses in the heat stability 0/ the photosynthetic apparatus .......................... CONCLUDING REMARKS ...................................................................................... ........................................................................................................

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IC.I.W.-C.P.B. Publication No. 673. 491

0066-4294/80/0601-0491$01.00

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BERRY

& BJORKMAN

INTRODUCTION Temperature is prominent among the major tcological variables that deter­ mine the natural distribution of plants. Habitats occupied by higher plants show dramatic differences in the prevailing temperature during the period of active growth, ranging from near freezing in certain arctic and alpine environments to over

50°C in the hottest deserts. Moreover, in many habi­

Annu. Rev. Plant. Physiol. 1980.31:491-543. Downloaded from arjournals.annualreviews.org by Stanford University - Main Campus - Green Library on 05/05/10. For personal use only.

tats the same plant individual is subjected to a very wide seasonal variation in temperature regime and even diurnal temperature fluctuation can be considerable. Like almost all other growth processe:., photosynthesis is strongly affected by temperature. In most plants, chllnges in photosynthetic rate in response to temperature are reversible over a considerable range (commonly

10° to 35°C), but exposure to temperatures l:>elow or above this range may cause irreversible injury to the photosynthetic system. Thus, in addition to the effect of temperature on photosynthesis arising from the intrinsic tem­

perature dependence of the process in the mnge over which the functional

integrity of the photosynthetic apparatus remains intact, extreme tempera­ tures can drastically inhibit photosynthesis by disrupting the integrity of the system. Higher plants from thermally contrasting habitats show considerable

differences in their photosynthetic respons�: to temperature, and especially in their ability to maintain functional integrity at low and high temperature

extremes. Such adaptations may be considE!red as a genotypic variation in key constituents of the photosynthetic appa.ratus, enabling plants to func­ tion efficiently under the temperature regimes of their various native habi­

tats. In addition, certain plants possess considerable phenotypic plasticity in their photosynthetic characteristics. Growth of a given genotype under a cool regime results in an improved photosynthetic capacity at low temper­ ature whereas growth under a warm regime results in an imprOVed photo­

synthetic performance at high temperatures. The potential for such photosynthetic acclimation to growth temp�rature is quite variable between species. The purpose of this review is to discuss n:cent advances in our knowledge of the effect of temperature on the photosynthetic process as it occurs in higher plant leaves, to evaluate the extent of photosynthetic temperature adaptation in higher plants, and to consiCler the underlying physiological and biochemical mechanisms. Our treatment is limited to levels of organiza­ tional complexity ranging from single leaft isolated chloroplasts or chloro­ plast constituents. The relaxation times of the responses under

consideration will vary from less than a second to several months. Consider­ ation of other important aspects such as the heat exchange between plant

TEMPERATURE RESPONSE OF PHOTOSYNTHESIS

493

canopies and the environment, the effect of temperature on photosynthate partitioning, and on whole plant productivity, as well as freezing injury, and the interactions between the effects temperature and water stress on whole plant photosynthesis are outside the scope of this review.

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ECOLOGICAL ASPECTS OF PHOTOSYNTHETIC TEMPERATURE ADAPTATION There are numerous reports in the literature on the temperature response of net CO2 exchange determined on a variety of species in a diversity of natural and variously modified environments. Our review of this largely descriptive research is not exhaustive and with some exceptions covers only the past 10 years. Pisek (158) has provided an extensive treatment of most of the earlier work in this field. Osmond, Bjorkman & Anderson (147) have provided a treatment of photosynthetic response to environmental factors in the context of plant physiological ecology. Unfortunately, attempts to compare the results obtained by different investigators on different species and in different environments suffer from the problems that the temperature dependence of photosynthesis, even for a single leaf, is strongly influenced by other environmental factors. As discussed in detail in a later section, light intensity and intercellular CO2 pressure have especially pronounced effects. The temperature dependence of photosynthesis becomes increasingly pronounced in the case that either light or intercellular CO2 level is increased. Because of its influence on intercellular CO2 pressure, stomatal conductance greatly affects the temper­ ature response of photosynthesis. Only rarely is there sufficient information to permit an assessment of the effect of these interacting factors in compari­ sons of the temperature-related characteristics of photosynthesis among species, especially in natural situations. Such comparisons are further com­ plicated by the fact that these characteristics are also influenced by the previous history of the plant. Not only does the growth temperature affect the temperature response of photosynthesis, but also leaf age and the light, water, and nutrient regimes to which the plant has been subjected have a marked influence, either by directly affecting the intrinsic photosynthetic properties or indirectly by affecting stomatal conductance. Photosynthetic Temperature Dependence in Thermally Contrasting Climates In spite of the complications mentioned above, it is nevertheless clear that plants occupying thermally contrasting habitats generally exhibit photosyn­ thetic temperature responses that reflect an adaptation to the temperature regimes of their respective habitats. Plants which are native to and grown

BERRY & BJORKMAN

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in cool environments generally exhibit high(:r photosynthetic rates at low

temperatures, and optimum p hoto synthetic rates occur at lower tempera­ tures in comparison with plants which are native to and grown in warm environments. Conversely, the latter plants exhibit a superior photosyn­ thetic performance at high temperatures, in large part as a result of an increased heat stability of the photosyntheti.c apparatus.

Annu. Rev. Plant. Physiol. 1980.31:491-543. Downloaded from arjournals.annualreviews.org by Stanford University - Main Campus - Green Library on 05/05/10. For personal use only.

The two types of responses are illustrated in Figure I (38), which com­

pares the temperature dependence of photosynthesis of Atrip/ex g/abriu­

scu/a, native to and grown in a cool coastal environment, with that of Tidestromia ob/ongifolia, a summer-active, winter-dormant species native to and grown in the extremely hot desert of Death V alley , California (40). Photosynthesis measurements were made under similar conditions of high light and normal atmospheric CO2 and O2 levels, and simultaneous determi­ nations of stomatal conductance showed that stomatal factors were in no

part responsible for the differences in photosynthetic temperature depen-

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TEMPERATURE RESPONSE OF PHOTOSYNTHESIS

495

dence between the two species. The cool coastal species has high photosyn­ thetic rates in the 10° to 20°C range, very much superior to those of the hot desert species. By contrast, the desert species is greatly superior at high temperatures. It continues to increase its photosynthetic rate as temperature is increased over a wide range, and the temperature optimum does not occur until 46°C. This temperature causes irreversible inhibition of photosyn­ thetic activity in the coastal species.

Annu. Rev. Plant. Physiol. 1980.31:491-543. Downloaded from arjournals.annualreviews.org by Stanford University - Main Campus - Green Library on 05/05/10. For personal use only.

Comparison with field studies on a number of other unrelated species occupying cool coastal environments (H. A. Mooney, unpublished) indi­ cates that the photosynthetic temperature dependence of A. glabriuscula, shown in Figure 1, provides a good representation for such plants. Species possessing the C4 dicarboxylic acid pathway of CO2 fixation (C4 species) tend to exhibit higher optimum temperatures for photosynthesis at normal air levels of CO2 than do species lacking this pathway (C3 species). The underlying reasons for this difference are discussed later. In accordance with this generalization, the cold-adapted C4 plant Atriplex sabulosa is capable of high photosynthetic rates at higher temperatures than A. glabri­

uscula (C3), with which it frequently coexists in cool strand habitats both in northern Europe and northeastern North America. Nevertheless, the photosynthetic capacity at low temperatures of these two C3 and C4 species are similarly high, and neither species possess a high heat tolerance (38; cf Figure

2).

Comparisons of a number of investigations on a wide diversity of higher

plant species from cool-temperature environments, conducted either in the native sites or on plants grown under a cool temperature regime simulating the native habitat (e.g. 1,23,38,39,72,89,140, 187-191, 196,217), indicate that the temperature response curves for photosynthesis are rather similar

in shape, generally resembling that shown in Figure I for A. glabriuscula,

although there is a tendency for a shift in the position of the optimum temperature in concert with the habitat or growth temperature, and the maximum photosynthetic rate may exhibit large differences among species. Similar temperature-dependence curves have also been found in desert winter annuals and in C3 evergreen desert perennials during the cool season or when grown under a cool temperature regime (30, 54, 111, 128, 130,

131). Not even cold-adapted plants such as Oxyria digyna from extreme envi­

ronments such as arctic Ellesmere Island at 82° north latitude or alpine San

Francisco Peak in Arizona at 3414 m altitude reach their optimum tempera­ ture for photosynthesis unti11° 5

curves are broad, permitting rates to remain at L 75% of the maximum

over a range extending from 10° to 30°C (23). Field studies on several mosses growing in the oceanic-arctic habitat of Barrow, Alaska (71° north

496

BERRY & BJORKMAN

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