Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor L. Moench)

Abstract

High temperature stress-induced male sterility is a critical problem in grain sorghum (Sorghum bicolor L. Moench) that significantly compromises crop yields. Grain sorghum plants were grown season-long under ambient (30/20 degrees C, day-time maximum/night-time minimum) and high temperature (36/26 degrees C) conditions in sunlit Soil-Plant-Atmospheric-Research (SPAR) growth chambers. We report data on the effects of high temperature on sugar levels and expression profiles of genes related to sugar-to-starch metabolism in microspore populations represented by pre- and post-meiotic "early" stages through post-mitotic "late" stages that show detectable levels of starch deposition. Microspores from high temperature stress conditions showed starch-deficiency and considerably reduced germination, translating into 27% loss in seed-set. Sugar profiles showed significant differences in hexose levels at both "early" and "late" stages at the two temperature regimes; and most notably, undetectable sucrose and approximately 50% lower starch content in "late" microspores from heat-stressed plants. Northern blot, quantitative PCR, and immunolocalization data revealed a significant reduction in the steady-state transcript abundance of SbIncw1 gene and CWI proteins in both sporophytic as well as microgametophytic tissues under high temperature conditions. Northern blot analyses also indicated greatly altered temporal expression profiles of various genes involved in sugar cleavage and utilization (SbIncw1, SbIvr2, Sh1, and Sus1), transport (Mha1 and MST1) and starch biosynthesis (Bt2, SU1, GBSS1, and UGPase) in heat-stressed plants. Collectively, these data suggest that impairment of CWI-mediated sucrose hydrolysis and subsequent lack of sucrose biosynthesis may be the most upstream molecular dysfunctions leading to altered carbohydrate metabolism and starch deficiency under elevated growth temperature conditions.

Response of floret fertility and individual grain weight of wheat to high temperature stress: sensitive stages and thresholds for temperature and duration

“…In addition, morphological characters such as stigma hyperplasia and stamen hypoplasia can result in failure of pollination (contact of pollen with stigma) and the fertilisation process (Takeoka et al 1991). Changes in composition and concentrations of carbohydrates (Jain et al 2007), lipids and reactive oxygen species (Djanaguiraman et al 2013a(Djanaguiraman et al , 2013b(Djanaguiraman et al , 2014 in pollen gains result in pollen sterility. Additional research is required to test these principles in wheat.…”

Sensitivity of flowering plant gametophytes to temperature fluctuations

“…Likewise, the analysis of carbohydrate content in chickpea flowers subjected to cold stress revealed a reduction in carbohydrate levels in aborted styles and ovaries compared to those retained in the plant (Nayyar et al, 2005). Recently, Jain et al (2007) found a disruption in cell wall invertase activity under low temperature stress not only during the commonly reported pollen developmental phase but also in the stigma and the style. Taken together, these findings point out to a plausible effect of temperature stress on the sporophytic structures of the pistil and warrant further research.…”

“…A c c e p t e d M a n u s c r i p t 9 turnover in developing pollen grains, and, hence, lower accumulation of soluble carbohydrates (Aloni et al, 1991;Jain et al, 2007;Oliver et al, 2005;Pressman et al, 2002;Sato et al, 2002). A complete understanding of temperature stress on pollen development must await further understanding of carbohydrate turnover during this phase.…”

Starch distribution in anthers, microspores and pollen grains in Aechmea recurvata (Klotzsch.) L.B.Sm., Dyckia racinae L.B.Sm. and Tillandsia aeranthos (Loisel.) L.B.Sm. (Bromeliaceae)

“…PAS-positive polysaccharides were found in the mature pollen grains cytoplasm in Mercurialis annua and Ricinus communis (Franchi et al 1996), and in Trachycarpus fortunei . Soluble polysaccharides are also found in mature starchless pollen grains, but they are only detected using other methodologies, especially biochemical analyses (O'Brien & McCully 1981;Pacini 1996;Castro & Clément 2007;Speranza et al 1997;Jain et al 2007). Speranza et al (1997) and Clément & Pacini (2001) demonstrated that, for different species, the PAS-positive cytoplasm of the vegetative cells is closely related to pollen grains dehydration at the time of their release, which presents a great viability after they are released, and are always associated with a dry environment.…”