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

Abstract 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 gen...

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Main Authors: Ali Soltani, Katelynn A. Walter, Andrew T. Wiersma, James P. Santiago, Michelle Quiqley, Daniel Chitwood, Timothy G. Porch, Phillip Miklas, Phillip E. McClean, Juan M. Osorno, David B. Lowry
Format: Article
Language:English
Published: BMC 2021-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-021-02837-6
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author Ali Soltani
Katelynn A. Walter
Andrew T. Wiersma
James P. Santiago
Michelle Quiqley
Daniel Chitwood
Timothy G. Porch
Phillip Miklas
Phillip E. McClean
Juan M. Osorno
David B. Lowry
author_facet Ali Soltani
Katelynn A. Walter
Andrew T. Wiersma
James P. Santiago
Michelle Quiqley
Daniel Chitwood
Timothy G. Porch
Phillip Miklas
Phillip E. McClean
Juan M. Osorno
David B. Lowry
author_sort Ali Soltani
collection DOAJ
description Abstract 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.
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spelling doaj.art-5e366b1bb5ce4100afb97d852e1008042022-12-21T21:56:24ZengBMCBMC Plant Biology1471-22292021-01-0121111710.1186/s12870-021-02837-6The genetics and physiology of seed dormancy, a crucial trait in common bean domesticationAli Soltani0Katelynn A. Walter1Andrew T. Wiersma2James P. Santiago3Michelle Quiqley4Daniel Chitwood5Timothy G. Porch6Phillip Miklas7Phillip E. McClean8Juan M. Osorno9David B. Lowry10Plant Resilience Institute, Michigan State UniversityPlant Resilience Institute, Michigan State UniversityDepartment of Plant, Soil and Microbial Sciences, Michigan State UniversityPlant Resilience Institute, Michigan State UniversityDepartment of Horticulture, Michigan State UniversityDepartment of Horticulture, Michigan State UniversityUSDA-ARS, Tropical Agriculture Research StationUSDA-ARS, Grain Legume Genetics Physiology Research UnitDepartment of Plant Sciences, North Dakota State UniversityDepartment of Plant Sciences, North Dakota State UniversityPlant Resilience Institute, Michigan State UniversityAbstract 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.https://doi.org/10.1186/s12870-021-02837-6Common beanDomesticationDormancyGerminationImbibitionPectin
spellingShingle Ali Soltani
Katelynn A. Walter
Andrew T. Wiersma
James P. Santiago
Michelle Quiqley
Daniel Chitwood
Timothy G. Porch
Phillip Miklas
Phillip E. McClean
Juan M. Osorno
David B. Lowry
The genetics and physiology of seed dormancy, a crucial trait in common bean domestication
BMC Plant Biology
Common bean
Domestication
Dormancy
Germination
Imbibition
Pectin
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 Common bean
Domestication
Dormancy
Germination
Imbibition
Pectin
url https://doi.org/10.1186/s12870-021-02837-6
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