Journal of Experimental Botany, Vol. 49, No. 326, pp. 1519–1528, September 1998
Effects of alien cytoplasmic variation on carbon assimilation and productivity in wheat Peter Jones1,3, Eavan M. Keane1 and Bruce A. Osborne2 1Department of Plant Science, University College Cork, Cork, Ireland 2Department of Botany, University College Dublin, Belfield, Dublin 4, Ireland Received 2 January 1998; Accepted 30 April 1998
Abstract In glasshouse studies of four alloplasmic wheat series, phenotypic characters were least affected when the recipient parent cytoplasm was replaced by donor cytoplasm of the S or D plasmatype. In the T. aestivum cv. ‘Selkirk’ series, cytoplasm substitution did not affect P per unit leaf area, although the flag leaf max area (and photosynthetic rate per leaf ) of each alloplasmic line was greater than that of euplasmic ‘Selkirk’. In field trials, all the D plasmatype alloplasmics tested produced more ears m−2 than did euplasmic ‘Selkirk’. The increased tiller number and leaf area of alloplasmic lines resulted in greater canopy light interception than euplasmic ‘Selkirk’ early in the season. This characteristic was associated with reduced weed populations under crops of alloplasmic ‘Selkirk’ lines grown under low-, but not high-input, agronomic regimes, with Ae. cylindrica– and Ae. ventricosa– ‘Selkirk’ significantly outyielding alloplasmic ‘Selkirk’ under low-input conditions. The F populations from 2 crosses between European wheat varieties and ‘Selkirk’ lines exhibited higher standard deviations for grain yield for alloplasmic than for euplasmic ‘Selkirk’, suggesting potential for selecting heterotic nuclear– cytoplasmic combinations with alien cytoplasms. Key words: Alien photosynthesis.
cytoplasmic
variation,
wheat,
Introduction In wheat (Triticum aestivum L.), alien cytoplasm substitution (resulting in alloplasmic lines) has been reported to produce agronomically valuable changes in a range of phenotypic traits, including plant height, flowering date
(Busch and Maan, 1978), cold resistance (Cahalan and Law, 1979), disease resistance ( Washington and Maan, 1974), and disease tolerance ( Keane and Jones, 1990). In contrast, the effects of alien cytoplasms on grain yield have been reported to be largely detrimental ( Kihara, 1973; Law and Worland, 1984). The principal trait affecting grain yield in wheat alloplasmics has been cytoplasmic male-sterility, although certain alloplasmic lines have been shown to exhibit potentially valuable alterations in some of the components of economic yield, such as ear number ( Fujigaki and Tsunewaki, 1979), dry matter production (Hori and Tsunewaki, 1969), 1000 grain weight (Jost et al., 1975), and spikelet number per ear (Netevic and Sanduhaz, 1968). Most studies utilizing alien cytoplasms in wheat improvement have centred on their use as inducers of cytoplasmic male-sterility for F hybrid wheat breeding 1 programmes ( Wilson and Ross, 1962; Edwards, 1983; Wilson and Driscoll, 1983). A number of researchers, however, have investigated the possibility of using fertile alloplasmic wheat lines to achieve nuclear–cytoplasmic heterosis, with alloplasmic lines out-yielding the two euplasmic parents (which contain nuclear and cytoplasmic genomes from the same source). This has led to the development of two contrasting strategies, with an emphasis on either cytoplasms from species distantly related to T. aestivum (to introduce a wider range of effects; Yonezawa et al., 1986), or alternatively, on cytoplasms from species closely related to T. aestivum (to minimize detrimental effects; Sasakuma and Ohtsuka, 1979). Results from this research have been equivocal. Several groups, particularly those studying cytoplasms from species closely related to T. aestivum, have reported heterosis ( Kihara, 1973; Panayotov and Gotsov, 1973), while others did not ( Edwards, 1983; Yonezawa et al., 1986).
3 To whom correspondence should be addressed. Fax: +353 21 274420. E-mail:
[email protected] © Oxford University Press 1998
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In plants, the cytoplasmic genomes, the chondriome (containing approximately 120–140 genes; Sugiura, 1992) in the mitochondria, and the plastome (95–100 genes; Schuster and Brennicke, 1994) in the plastids, carry genes which code predominantly for components of the gene expression machinery (tRNA and rRNA) and for membrane-bound proteins involved in organelle-specific metabolism. The transfer, during evolution, of many cytoplasmic genes to the nuclear genomes has resulted in the dependence of mitochondria and plastids on the import of nuclear-encoded proteins to carry out organelle biogenesis and photosynthesis (chloroplasts) or respiration (mitochondria). This, in turn, necessitates modulation of cytoplasmic and nuclear gene expression, as illustrated by the co-ordinated expression of the plastid-encoded rbc L gene (coding for the large subunit) and the nuclear-encoded rbc S gene (for the small subunit) responsible for Rubisco synthesis. This inter-genomic regulation of gene expression is achieved by the involvement in the control of cytoplasmic gene expression of nuclear-encoded gene products including key structural and enzymatic factors vital for organellar function, and regulatory factors, such as those controlling plastid mRNA translation (Gillham et al., 1994). Given the involvement of both cytoplasmic and nuclear genes in controlling carbon metabolism, the replacement of parental chloroplast and mitochondrial genomes with those from related species may be expected to impact on photosynthesis and respiratory metabolism, either directly or via modified nuclear–cytoplasmic interaction. Little has been published in this area, although Evans (1986) reported that an alloplasmic wheat line containing Triticum boeoticum cytoplasm expressed only 71% of the in vitro Rubisco activity exhibited by the euplasmic (T. aestivum cytoplasm) line. The objective of this research was to investigate the effect of alien cytoplasms on carbon metabolism and productivity of wheat in the glasshouse and in the field under northern European conditions.
Materials and methods Plant material The cytoplasm donors of the alloplasmic series based on T. aestivum cv. Chinese Spring ( Table 1) and T. aestivum cv. Chris, cv. Selkirk and T. durum (Table 2) are given in the relevant tables. These series were developed by Professor K Tsunewaki, Kyoto University, Japan (‘Chinese Spring’ series) and Professor SS Maan, North Dakota State University, USA (T. durum, ‘Chris’ and ‘Selkirk’ series) by crossing the euplasmic line (as pollen parent) with the cytoplasmic donor (as egg parent) and then back-crossing (generally for more than ten generations) the hybrid (as female parent) to the recurrent euplasmic line.
Pot experiments Plants were grown in a peat-based compost in 12.5 cm pots (two plants per replicate pot, eight replicates per genotype) in a glasshouse with supplementary lighting, giving maximum irradiances of 880 mmol m−2 s−1 with a photoperiod of 16 h and a temperature range of 18–25 °C. Plants were fed weekly with half-strength Hoagland’s nutrient solution, with regular flushing of the pots to prevent accumulation of salts. Field experiments Plants were grown in 1×1 m (F material ) or 2×2 m microplots 2 (other trials), at a plant density of 250 plants m−2, with four replicates per treatment in a replicated randomized block design. Fertilizer was applied to a total of 150 kg nitrogen ha−1, in two splits (50 kg nitrogen ha−1 as 10:10:15 in the seed bed and 100 kg nitrogen ha−1 as calcium ammonium nitrate at GS30; Zadoks et al., 1974), unless stated to the contrary. To prevent lodging, plants were supported by allowing them to grow through 10×10 cm mesh netting. Fungicide and herbicide applications were routinely made as used for the high-input regime (described below), unless stated otherwise. In the experiment comparing the field performance of alloplasmic and euplasmic ‘Selkirk’ lines under high- and lowinput regimes, the former involved 200 kg nitrogen ha−1, a three-spray fungicide programme (at first node (GS31), flag leaf emergence (GS39) and anthesis (GS66; Zadoks et al., 1974), using ‘Tilt C’ (Ciba-Geigy; active ingredients (a.i.) propiconazole and carbendazim) at the manufacturer’s recommended rate, and a post-emergence herbicide treatment with ‘Ally’ (Du Pont; a.i. metsulphuron-methyl ) at the manufacturer’s recommended rate, at the fourth leaf stage. In the lowinput regime, the agrochemical treatments were adjusted to 80 kg nitrogen ha−1, a one-spray fungicide programme (at flag leaf emergence) at the recommended rate, and a post-emergence herbicide application made at one-quarter the recommended rate. In both regimes, 50 kg nitrogen ha−1 was applied in the seed bed, with the remainder at GS30. Weed biomass (aboveground tissue) was harvested from each microplot at crop maturity, dried at 65 °C for 48 h and then weighed. Measurements Unless otherwise stated, all measurements on pot-grown plants were conducted on tissues of the main stem. Measurements in microplots were conducted on the whole plants (main stem plus tillers). Weights were determined after plant material was dried at 65 °C for 48 h. Light interception measurements In the study of four alloplasmics and the euplasmic ‘Selkirk’ line, light interception by the crop canopy was measured between 12.00 h and 14.15 h at 15 dates throughout the growing season. Six sites were selected at random at the base of each microplot and the amount of photosynthetically active radiation (PAR) was measured at each site on each date, using a PAR sensor and meter (Skye Instruments, Llandrindod Wells, Powys, UK ). These values were converted into percentage light interception by reference to incident PAR measurements above the canopy. Light interception during three phases of crop development (GS1–GS30, GS31–GS65 and GS66–GS99) was obtained by integration of the ‘% light interception versus time’ curve, using the trapezoid method, and expressed as Area Under the Light Interception Curve (AULIC ).
Table 1. Morphological and developmental traits in the T. aestivum cv. Chinese Spring alloplasmic series All traits except tiller number refer to the main shoot of the pot-grown plants. The absolute value is presented for euplasmic ‘Chinese Spring’ (T. aestivum cytoplasm); values for alloplasmic lines are presented as % euplasmic value. An asterisk indicates a significant difference (P
