Loss of physical seed dormancy, a major domestication trait in common bean, is likely caused by a single loss-of-function mutation

Authors: SOLTANI, ALI - Michigan State University; WALTER, KATELYNN - Michigan State University; WIERSMA, ANDREW - Michigan State University; SANTIAGO, JAMES - Michigan State University; QUIQLEY, MICHELLE - Michigan State University; CHITWOOD, DAN - Michigan State University; SHARKEY, THOMAS - Michigan State University; Porch, Timothy - Tim; Miklas, Phillip - Phil; MCCLEAN, PHILLIP - North Dakota State University; OSORNO, JUAN - North Dakota State University; LOWRY, DAVID - Michigan State University

Submitted to: BMC Plant Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/11/2021
Publication Date: 1/22/2021
Citation: Soltani, A., Walter, K.A., Wiersma, A., Santiago, J.P., Quiqley, M., Chitwood, D., Sharkey, T.D., Porch, T.G., Miklas, P.N., McClean, P.E., Osorno, J.M., Lowry, D.B. 2021. Loss of physical seed dormancy, a major domestication trait in common bean, is likely caused by a single loss-of-function mutation. Biomed Central (BMC) Plant Biology. 21, Article 58. https://doi.org/10.1186/s12870-021-02837-6.
DOI: https://doi.org/10.1186/s12870-021-02837-6

Interpretive Summary: Physical seed dormancy is an important trait in legume domestication. Although seed dormancy is beneficial in wild ecosystems, it is an undesirable trait in crops. Here we employed an integrative approach to understand the mechanisms controlling physical seed dormancy in common bean. Using an innovative CT-scan imaging system, we tracked water inside the seed coat of common bean seeds. Further, we performed a genetic quantitative trait loci (QTL) analysis and subsequent fine-mapping to narrow down the position of the gene in the bean genome. We also conducted gene expression and mutational polymorphism analysis to narrow down the list of likely causative genes. We found that water uptake initiates from the bean lens, a physical structure on the common bean seed. Genetic analysis revealed that water uptake is associated with a single major QTL on chromosome Pv03. Further analysis indicates that a 5-basepair insertion in an ortholog of pectin acetylesterase-8 is likely the major causative mutation underlying the loss of seed dormancy. Our findings indicate that seed coat dormancy is likely associated with pectin structure that affects cell wall adhesion of common bean seed. The 5-bp insertion in pectin acetylesterase-8 results in looser cell walls, which facilitates water uptake. A drastic difference in the haplotype frequency between wild and domesticated beans suggests that this variant was under strong selection pressure during domestication. Seed dormancy has potential applications in common bean production in areas with excessive precipitation or flooding during the planting season.

Technical Abstract: Physical seed dormancy is an important trait in legume domestication. Although seed dormancy is beneficial in wild ecosystems, it is an undesirable trait in crops. Here we employed an integrative approach to understand the mechanisms controlling physical seed dormancy in common bean (Phaseolus vulgaris L.). Using an innovative CT-scan imaging system, we tracked water inside the seed coat. Further, we performed a QTL analysis and subsequent fine-mapping to narrow down the position of the causative mutation/gene. We conducted gene expression and mutational polymorphism analysis to narrow down the list of likely causative genes. We found that water uptake initiates from the bean lens. Genetic analysis revealed that the water uptake is associated with a single major QTL on Pv03. Further analysis indicates that a 5-bp insertion in an ortholog of pectin acetylesterase-8 is likely a major causative mutation underlying the loss of seed dormancy. Our findings indicate that seed coat dormancy is likely associated with pectin structure that affects cell wall adhesion. The 5-bp insertion in pectin acetylesterase-8 results in looser cell walls, which facilitates water uptake. A drastic difference in the haplotype frequency between wild and domesticated beans suggests that this variant was under strong selection pressure during domestication.