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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°C, day-time maximum/night-time minimum) and high temperature (36/26°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 ∼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.

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Abbreviations

ADP-Glc:

Adenine 5′-diphosphate-glucose

AGPase:

ADP-pyrophosphorylase

Bt2 :

Brittle 2

CWI:

Cell wall invertase

DAS:

Days-after-sowing

Frc:

Fructose

GBSS1 :

Granule bound starch synthase-1

Glc:

Glucose

INCW:

Cell wall invertase protein

Mha1 :

Plasma membrane H+ATPase gene

MST1 :

Monosaccharide transporter gene

SbIncw1 :

Sorghum cell wall invertase gene

SbIvr2 :

Sorghum vacuolar invertase gene

Sh1 :

Shrunken 1

SU1 :

Sugary 1

Suc:

Sucrose

Sus1 :

Sucrose synthase 1

SuSy :

Sucrose synthase

UDP-Glc:

Uridine 5′-diphosphate-glucose

UGPase :

UDP-pyrophosphorylase gene

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Acknowledgments

Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. We thank Drs. D. R. Pring and C. L. Guy for critical reading of the manuscript and Mr. A. Funk for excellent technical assistance. This work was supported in part by the US Department of Agriculture (USDA)-Agricultural Research Service (ARS) and by the United States-Israel Binational Agricultural Research and Development Fund (grant no. IS-3738-05 R). It was a cooperative investigation between USDA-ARS and the Institute of Food and Agricultural Science, University of Florida.

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Correspondence to Prem S. Chourey.

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Jain, M., Prasad, P.V.V., Boote, K.J. et al. Effects of season-long high temperature growth conditions on sugar-to-starch metabolism in developing microspores of grain sorghum (Sorghum bicolor L. Moench). Planta 227, 67–79 (2007). https://doi.org/10.1007/s00425-007-0595-y

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Keywords

  • Cell wall invertase
  • Grain sorghum
  • Heat stress
  • Microsporogenesis
  • Pollen sterility
  • Starch biosynthesis