FLOWERING LOCUS C (FLC) is a major regulator of flowering responses to seasonal environmental factors. Here, we document that FLC also regulates another major life-history transition-seed germination, and that natural variation at the FLC locus and in FLC expression is associated with natural variation in temperaturedependent germination. FLC-mediated germination acts through additional genes in the flowering pathway (FT, SOC1, and AP1) before involving the abscisic acid catabolic pathway (via CYP707A2) and gibberellins biosynthetic pathway (via GA20ox1) in seeds. Also, FLC regulation of germination is largely maternally controlled, with FLC peaking and FT, SOC1, and AP1 levels declining at late stages of seed maturation. High FLC expression during seed maturation is associated with altered expression of hormonal genes (CYP707A2 and GA20ox1) in germinating seeds, indicating that gene expression before the physiological independence of seeds can influence gene expression well after any physical connection between maternal plants and seeds exists. The major role of FLC in temperature-dependent germination documented here reveals a much broader adaptive significance of natural variation in FLC. Therefore, pleiotropy between these major life stages likely influences patterns of natural selection on this important gene, making FLC a promising case for examining how pleiotropy influences adaptive evolution.life history ͉ pleiotropy ͉ vernalization ͉ natural variation ͉ FRIGIDA
Seasonal germination timing of Arabidopsis thaliana strongly influences overall life history expression and is the target of intense natural selection. This seasonal germination timing depends strongly on the interaction between genetics and seasonal environments both before and after seed dispersal. DELAY OF GERMINATION 1 (DOG1) is the first gene that has been identified to be associated with natural variation in primary dormancy in A. thaliana. Here, we report interaccession variation in DOG1 expression and document that DOG1 expression is associated with seed-maturation temperature effects on germination; DOG1 expression increased when seeds were matured at low temperature, and this increased expression was associated with increased dormancy of those seeds. Variation in DOG1 expression suggests a geographical structure such that southern accessions, which are more dormant, tend to initiate DOG1 expression earlier during seed maturation and achieved higher expression levels at the end of silique development than did northern accessions. Although elimination of the synthesis of phytohormone abscisic acid (ABA) results in the elimination of maternal temperature effects on dormancy, DOG1 expression predicted dormancy better than expression of genes involved in ABA metabolism.
Summary• Environmental conditions during seed maturation influence germination, but the genetic basis of maternal environmental effects on germination is virtually unknown.• Using single and multiple mutants of phytochromes, it is shown here that different phytochromes contributed to germination differently, depending on seed-maturation conditions.• Arabidopsis thaliana wild-type seeds that were matured under cool temperatures were intensely dormant compared with seeds matured at warmer temperature, and this dormancy was broken only after warm seed-stratification followed by cold seedstratification. The warm-cold stratification broke dormancy in fresh seeds but not in dry after-ripened seeds. Functional PHYB and PHYD were necessary to break cool-induced dormancy, which indicates a previously unknown and ecologically important function for PHYD. Disruption of PHYA in combination with PHYD (but not PHYB) restored germination to near wild-type levels, indicating that PHYA contributes to the maintenance of cool-induced dormancy on a phyD background. Effects of seed-maturation temperature were much stronger than effects of seed-maturation photoperiod. PHYB contributed to germination somewhat more strongly in seeds matured under short days, whereas PHYD contributed to germination somewhat more strongly in seeds matured under long days.• The variable contributions of different phytochromes to germination as a function of seed-maturation conditions reveal further functional diversification of the phytochromes during the process of germination. This study identifies among the first genes to be associated with maternal environmental effects on germination.
Knowledge of the upper limits of temperature tolerance is essential to understand how tropical trees will respond to global warming. We quantified leaf thermotolerance in 41 tree species growing in a seasonally dry tropical region of the Indian subcontinent to examine: (1) differences between evergreen and deciduous species; (2) relationships with leaf mass per area (LMA) and leaf size; and, (3) seasonal variation in thermotolerance. Thermotolerance ranged from 45.5 °C to 50.5 °C among species, was higher for evergreen than deciduous species, and was negatively related to a continuous estimate of deciduousness. Species with higher LMA had higher thermotolerance, but we did not detect any relationship between leaf size and thermotolerance. Seasonal changes in thermotolerance varied among species implying that species’ capacity to acclimate may differ. Thermal safety margins, the difference between thermotolerance and maximum habitat temperatures indicate that most species may be highly vulnerable to future warming. Overall our results show that deciduous, and fast growing species with low LMA are likely to be more negatively affected by global warming. This differential vulnerability may lead to directional changes in composition in dry tropical forests, and such changes could alter vegetation-atmosphere feedbacks and further exacerbate global warming.
Chloroplast small (low-molecular-weight) heat-shock proteins (csHsps) can protect photosynthetic electron transport (Pet), and quantitative variation in csHsps is correlated with thermotolerance of net photosynthesis and Photosystem II. However, the functional (i.e. protective) consequence of natural variation in csHsps is unknown. To investigate this, we used an in vitro assay to determine the contribution of csHsps to the tolerance of Pet to high temperatures in five ecotypes of Chenopodium album collected from habitats ranging from cool to warm, and we partitioned total Pet thermotolerance into basal and induced Pet components (without and with a pre-heat treatment, respectively, to induce csHsps). The ecotypes varied in total Pet thermotolerance and this was correlated with habitat temperature. Variation in total Pet thermotolerance was associated primarily with variation in induced Pet thermotolerance, and not with basal Pet thermotolerance. Variation in induced Pet was highly correlated with csHsp protection of Pet. Variation in csHsp function was associated with variation in csHsp content among ecotypes. These results are the first to demonstrate the direct functional consequences for natural variation in Hsps in plants, and show that functional variation is associated with evolutionary adaptation to specific habitats among ecotypes.
Production of heat-shock proteins (Hsps) is a key adaptation to acute heat stress and will be important in determining plant responses to climate change. Further, intraspecifc variation in Hsps, which will influence species-level response to global warming, has rarely been examined in naturally occurring plants. To understand intraspecific variation in plant Hsps and its relevance to global warming, we examined Hsp content and thermotolerance in five naturally occurring populations of Chenopodium album L. from contrasting thermal environments grown at low and high temperatures. As expected, Hsp accumulation varied between populations, but this was related more to habitat variability than to mean temperature. Unexpectedly, Hsp accumulation decreased with increasing variability of habitat temperatures. Hsp accumulation also decreased with increased experimental growth temperatures. Physiological thermotolerance was partitioned into basal and induced components. As with Hsps, induced thermotolerance decreased with increasing temperature variability. Thus, populations native to the more stressful habitats, or grown at higher temperatures, had lower Hsp levels and induced thermotolerance, suggesting a greater reliance on basal mechanisms for thermotolerance. These results suggest that future global climate change will differentially impact ecotypes within species, possibly by selecting for increased basal versus inducible thermotolerance.Key words: acclimation; photosynthesis; stress proteins; temperature. Barua D, Heckathorn SA, Coleman JS (2008). Variation in heat-shock proteins and photosynthetic thermotolerance among natural populations of Chenopodium album L. from contrasting thermal environments: implications for plant responses to global warming.
Determining effects of elevated CO 2 on the tolerance of photosynthesis to acute heat-stress (heat wave) is necessary for predicting plant responses to global warming, as photosynthesis is thermolabile and acute heat-stress and atmospheric CO 2 will increase in the future. Few studies have examined this, and past results are variable, which may be due to methodological variation. To address this, we grew two C 3 and two C 4 species at current or elevated CO 2 and three different growth temperatures (GT). We assessed photosynthetic thermotolerance in both unacclimated (basal tolerance) and preheat-stressed (preHS = acclimated) plants. In C 3 species, basal thermotolerance of net photosynthesis (P n ) was increased in high CO 2 , but in C 4 species, P n thermotlerance was decreased by high CO 2 (except Zea mays at low GT); CO 2 effects in preHS plants were mostly small or absent, though high CO 2 was detrimental in one C 3 and one C 4 species at warmer GT. Though high CO 2 generally decreased stomatal conductance, decreases in P n during heat stress were mostly due to non-stomatal effects. Photosystem II (PSII) efficiency was often decreased by high CO 2 during heat stress, especially at high GT; CO 2 effects on post-PSII electron transport were variable. Thus, high CO 2 often affected photosynthetic theromotolerance, and the effects varied with photosynthetic pathway, growth temperature, and acclimation state. Most importantly, in heat-stressed plants at normal or warmer growth temperatures, high CO 2 may often decrease, or not benefit as expected, tolerance of photosynthesis to acute heat stress. Therefore, interactive effects of elevated CO 2 and warmer growth temperatures on acute heat tolerance may contribute to future changes in plant productivity, distribution, and diversity.Key words: carbon dioxide; global climate change; photosynthesis; thermotolerance.Hamilton EW, Heckathorn SA, Joshi P, Wang D, Barua D (2008). Interactive effects of elevated CO 2 and growth temperature on the tolerance of photosynthesis to acute heat stress in C 3 and C 4 species.
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