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The genetics and physiology of seed dormancy, a crucial trait in common bean domestication

BACKGROUND: Physical seed dormancy is an important trait in legume domestication. Although seed dormancy is beneficial in wild ecosystems, it is generally considered to be an undesirable trait in crops due to reduction in yield and / or quality. The physiological mechanism and underlying genetic fac...

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Autores principales: Soltani, Ali, Walter, Katelynn A., Wiersma, Andrew T., Santiago, James P., Quiqley, Michelle, Chitwood, Daniel, Porch, Timothy G., Miklas, Phillip, McClean, Phillip E., Osorno, Juan M., Lowry, David B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7821524/
https://www.ncbi.nlm.nih.gov/pubmed/33482732
http://dx.doi.org/10.1186/s12870-021-02837-6
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author Soltani, Ali
Walter, Katelynn A.
Wiersma, Andrew T.
Santiago, James P.
Quiqley, Michelle
Chitwood, Daniel
Porch, Timothy G.
Miklas, Phillip
McClean, Phillip E.
Osorno, Juan M.
Lowry, David B.
author_facet Soltani, Ali
Walter, Katelynn A.
Wiersma, Andrew T.
Santiago, James P.
Quiqley, Michelle
Chitwood, Daniel
Porch, Timothy G.
Miklas, Phillip
McClean, Phillip E.
Osorno, Juan M.
Lowry, David B.
author_sort Soltani, Ali
collection PubMed
description BACKGROUND: Physical seed dormancy is an important trait in legume domestication. Although seed dormancy is beneficial in wild ecosystems, it is generally considered to be an undesirable trait in crops due to reduction in yield and / or quality. The physiological mechanism and underlying genetic factor(s) of seed dormancy is largely unknown in several legume species. Here we employed an integrative approach to understand the mechanisms controlling physical seed dormancy in common bean (Phaseolus vulgaris L.). RESULTS: Using an innovative CT scan imaging system, we were able to track water movements inside the seed coat. We found that water uptake initiates from the bean seed lens. Using a scanning electron microscopy (SEM) we further identified several micro-cracks on the lens surface of non-dormant bean genotypes. Bulked segregant analysis (BSA) was conducted on a bi-parental RIL (recombinant inbred line) population, segregating for seed dormancy. This analysis revealed that the seed water uptake is associated with a single major QTL on Pv03. The QTL region was fine-mapped to a 118 Kb interval possessing 11 genes. Coding sequence analysis of candidate genes revealed a 5-bp insertion in an ortholog of pectin acetylesterase 8 that causes a frame shift, loss-of-function mutation in non-dormant genotype. Gene expression analysis of the candidate genes in the seed coat of contrasting genotypes indicated 21-fold lower expression of pectin acetylesterase 8 in non-dormant genotype. An analysis of mutational polymorphism was conducted among wild and domesticated beans. Although all the wild beans possessed the functional allele of pectin acetylesterase 8, the majority (77%) of domesticated beans had the non-functional allele suggesting that this variant was under strong selection pressure through domestication. CONCLUSIONS: In this study, we identified the physiological mechanism of physical seed dormancy and have identified a candidate allele causing variation in this trait. Our findings suggest that a 5-bp insertion in an ortholog of pectin acetylesterase 8 is likely a major causative mutation underlying the loss of seed dormancy during domestication. Although the results of current study provide strong evidences for the role of pectin acetylesterase 8 in seed dormancy, further confirmations seem necessary by employing transgenic approaches. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02837-6.
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spelling pubmed-78215242021-01-22 The genetics and physiology of seed dormancy, a crucial trait in common bean domestication Soltani, Ali Walter, Katelynn A. Wiersma, Andrew T. Santiago, James P. Quiqley, Michelle Chitwood, Daniel Porch, Timothy G. Miklas, Phillip McClean, Phillip E. Osorno, Juan M. Lowry, David B. BMC Plant Biol Research Article BACKGROUND: Physical seed dormancy is an important trait in legume domestication. Although seed dormancy is beneficial in wild ecosystems, it is generally considered to be an undesirable trait in crops due to reduction in yield and / or quality. The physiological mechanism and underlying genetic factor(s) of seed dormancy is largely unknown in several legume species. Here we employed an integrative approach to understand the mechanisms controlling physical seed dormancy in common bean (Phaseolus vulgaris L.). RESULTS: Using an innovative CT scan imaging system, we were able to track water movements inside the seed coat. We found that water uptake initiates from the bean seed lens. Using a scanning electron microscopy (SEM) we further identified several micro-cracks on the lens surface of non-dormant bean genotypes. Bulked segregant analysis (BSA) was conducted on a bi-parental RIL (recombinant inbred line) population, segregating for seed dormancy. This analysis revealed that the seed water uptake is associated with a single major QTL on Pv03. The QTL region was fine-mapped to a 118 Kb interval possessing 11 genes. Coding sequence analysis of candidate genes revealed a 5-bp insertion in an ortholog of pectin acetylesterase 8 that causes a frame shift, loss-of-function mutation in non-dormant genotype. Gene expression analysis of the candidate genes in the seed coat of contrasting genotypes indicated 21-fold lower expression of pectin acetylesterase 8 in non-dormant genotype. An analysis of mutational polymorphism was conducted among wild and domesticated beans. Although all the wild beans possessed the functional allele of pectin acetylesterase 8, the majority (77%) of domesticated beans had the non-functional allele suggesting that this variant was under strong selection pressure through domestication. CONCLUSIONS: In this study, we identified the physiological mechanism of physical seed dormancy and have identified a candidate allele causing variation in this trait. Our findings suggest that a 5-bp insertion in an ortholog of pectin acetylesterase 8 is likely a major causative mutation underlying the loss of seed dormancy during domestication. Although the results of current study provide strong evidences for the role of pectin acetylesterase 8 in seed dormancy, further confirmations seem necessary by employing transgenic approaches. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02837-6. BioMed Central 2021-01-22 /pmc/articles/PMC7821524/ /pubmed/33482732 http://dx.doi.org/10.1186/s12870-021-02837-6 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Soltani, Ali
Walter, Katelynn A.
Wiersma, Andrew T.
Santiago, James P.
Quiqley, Michelle
Chitwood, Daniel
Porch, Timothy G.
Miklas, Phillip
McClean, Phillip E.
Osorno, Juan M.
Lowry, David B.
The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
title The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
title_full The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
title_fullStr The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
title_full_unstemmed The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
title_short The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
title_sort genetics and physiology of seed dormancy, a crucial trait in common bean domestication
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7821524/
https://www.ncbi.nlm.nih.gov/pubmed/33482732
http://dx.doi.org/10.1186/s12870-021-02837-6
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