Contrasting anther glucose‐6‐phosphate dehydrogenase activities between two bean varieties suggest an important role in reproductive heat tolerance

Common beans (Phaseolus vulgaris) are highly sensitive to elevated temperatures, and rising global temperatures threaten bean production. Plants at the reproductive stage are especially susceptible to heat stress due to damage to male (anthers) and female (ovary) reproductive tissues, with anthers b...

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Bibliographic Details
Published in:Plant, cell and environment cell and environment, 2021-07, Vol.44 (7), p.2185-2199
Main Authors: Santiago, James P., Soltani, Ali, Bresson, Madeline M., Preiser, Alyssa L., Lowry, David B., Sharkey, Thomas D.
Format: Article
Language:English
Subjects:
anther metabolism
Anthers
antioxidant enzymes
Antioxidants
BASIC BIOLOGICAL SCIENCES
Beans
Damage
Dehydrogenase
Dehydrogenases
Elevated temperature test
Enzymes
Genotypes
Glucose
Heat
Heat resistance
Heat stress
Heat tolerance
High temperature
Hydrogen peroxide
Hypotheses
Infertility
Leaves
Males
Original
Pentose
Pentose phosphate pathway
plant sciences
pollen development
reactive oxygen species
Reducing agents
ROS quenching
Scavenging
Sucrose
sucrose phloem loading
Temperature tolerance
Vegetables
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Summary:Common beans (Phaseolus vulgaris) are highly sensitive to elevated temperatures, and rising global temperatures threaten bean production. Plants at the reproductive stage are especially susceptible to heat stress due to damage to male (anthers) and female (ovary) reproductive tissues, with anthers being more sensitive to heat. Heat damage promotes early tapetal cell degradation, and in beans this was shown to cause male infertility. In this study, we focus on understanding how changes in leaf carbon export in response to elevated temperature stress contribute to heat‐induced infertility. We hypothesize that anther glucose‐6‐phosphate dehydrogenase (G6PDH) activity plays an important role at elevated temperature and promotes thermotolerance. To test this hypothesis, we compared heat‐tolerant and susceptible common bean genotypes using a combination of phenotypic, biochemical, and physiological approaches. Our results identified changes in leaf sucrose export, anther sugar accumulation and G6PDH activity and anther H2O2 levels and antioxidant‐related enzymes between genotypes at elevated temperature. Further, anther respiration rate was found to be lower at high temperature in both bean varieties. Overall, our results support the hypothesis that enhanced male reproductive heat tolerance involves changes in the anther oxidative pentose phosphate pathway, which supplies reductants to critical H2O2 scavenging enzymes. In this article, we describe the contribution of G6PDH in maintenance of ROS levels and by extension, its role in viable pollen production as a measure of heat tolerance in common beans. Our data indicate that continued flux of carbon through G6PDH in anthers helps remove hydrogen peroxide at high temperature in heat‐tolerant bean genotype.
ISSN:0140-7791
1365-3040
DOI:10.1111/pce.14057