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Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships

BACKGROUND: Climate change models predict more frequent incidents of heat stress worldwide. This trend will contribute to food insecurity, particularly for some of the most vulnerable regions, by limiting the productivity of crops. Despite its great importance, there is a limited understanding of th...

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Autores principales: Soltani, Ali, Weraduwage, Sarathi M., Sharkey, Thomas D., Lowry, David B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6480737/
https://www.ncbi.nlm.nih.gov/pubmed/31014227
http://dx.doi.org/10.1186/s12864-019-5669-2
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author Soltani, Ali
Weraduwage, Sarathi M.
Sharkey, Thomas D.
Lowry, David B.
author_facet Soltani, Ali
Weraduwage, Sarathi M.
Sharkey, Thomas D.
Lowry, David B.
author_sort Soltani, Ali
collection PubMed
description BACKGROUND: Climate change models predict more frequent incidents of heat stress worldwide. This trend will contribute to food insecurity, particularly for some of the most vulnerable regions, by limiting the productivity of crops. Despite its great importance, there is a limited understanding of the underlying mechanisms of variation in heat tolerance within plant species. Common bean, Phaseolus vulgaris, is relatively susceptible to heat stress, which is of concern given its critical role in global food security. Here, we evaluated three genotypes of P. vulgaris belonging to kidney market class under heat and control conditions. The Sacramento and NY-105 genotypes were previously reported to be heat tolerant, while Redhawk is heat susceptible. RESULTS: We quantified several morpho-physiological traits for leaves and found that photosynthetic rate, stomatal conductance, and leaf area all increased under elevated temperatures. Leaf area expansion under heat stress was greatest for the most susceptible genotype, Redhawk. To understand gene regulatory responses among the genotypes, total RNA was extracted from the fourth trifoliate leaves for RNA-sequencing. Several genes involved in the protection of PSII (HSP21, ABA4, and LHCB4.3) exhibited increased expression under heat stress, indicating the importance of photoprotection of PSII. Furthermore, expression of the gene SUT2 was reduced in heat. SUT2 is involved in the phloem loading of sucrose and its distal translocation to sinks. We also detected an almost four-fold reduction in the concentration of free hexoses in heat-treated beans. This reduction was more drastic in the susceptible genotype. CONCLUSIONS: Overall, our data suggests that while moderate heat stress does not negatively affect photosynthesis, it likely interrupts intricate source-sink relationships. These results collectively suggest a physiological mechanism for why pollen fertility and seed set are negatively impacted by elevated temperatures. Identifying the physiological and transcriptome dynamics of bean genotypes in response to heat stress will likely facilitate the development of varieties that can better tolerate a future of elevated temperatures. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5669-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-64807372019-05-01 Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships Soltani, Ali Weraduwage, Sarathi M. Sharkey, Thomas D. Lowry, David B. BMC Genomics Research Article BACKGROUND: Climate change models predict more frequent incidents of heat stress worldwide. This trend will contribute to food insecurity, particularly for some of the most vulnerable regions, by limiting the productivity of crops. Despite its great importance, there is a limited understanding of the underlying mechanisms of variation in heat tolerance within plant species. Common bean, Phaseolus vulgaris, is relatively susceptible to heat stress, which is of concern given its critical role in global food security. Here, we evaluated three genotypes of P. vulgaris belonging to kidney market class under heat and control conditions. The Sacramento and NY-105 genotypes were previously reported to be heat tolerant, while Redhawk is heat susceptible. RESULTS: We quantified several morpho-physiological traits for leaves and found that photosynthetic rate, stomatal conductance, and leaf area all increased under elevated temperatures. Leaf area expansion under heat stress was greatest for the most susceptible genotype, Redhawk. To understand gene regulatory responses among the genotypes, total RNA was extracted from the fourth trifoliate leaves for RNA-sequencing. Several genes involved in the protection of PSII (HSP21, ABA4, and LHCB4.3) exhibited increased expression under heat stress, indicating the importance of photoprotection of PSII. Furthermore, expression of the gene SUT2 was reduced in heat. SUT2 is involved in the phloem loading of sucrose and its distal translocation to sinks. We also detected an almost four-fold reduction in the concentration of free hexoses in heat-treated beans. This reduction was more drastic in the susceptible genotype. CONCLUSIONS: Overall, our data suggests that while moderate heat stress does not negatively affect photosynthesis, it likely interrupts intricate source-sink relationships. These results collectively suggest a physiological mechanism for why pollen fertility and seed set are negatively impacted by elevated temperatures. Identifying the physiological and transcriptome dynamics of bean genotypes in response to heat stress will likely facilitate the development of varieties that can better tolerate a future of elevated temperatures. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5669-2) contains supplementary material, which is available to authorized users. BioMed Central 2019-04-24 /pmc/articles/PMC6480737/ /pubmed/31014227 http://dx.doi.org/10.1186/s12864-019-5669-2 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Soltani, Ali
Weraduwage, Sarathi M.
Sharkey, Thomas D.
Lowry, David B.
Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships
title Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships
title_full Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships
title_fullStr Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships
title_full_unstemmed Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships
title_short Elevated temperatures cause loss of seed set in common bean (Phaseolus vulgaris L.) potentially through the disruption of source-sink relationships
title_sort elevated temperatures cause loss of seed set in common bean (phaseolus vulgaris l.) potentially through the disruption of source-sink relationships
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6480737/
https://www.ncbi.nlm.nih.gov/pubmed/31014227
http://dx.doi.org/10.1186/s12864-019-5669-2
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