Loss of pod strings in common bean is associated with gene duplication, retrotransposon insertion, and overexpression of PvIND

Abstract

Regulation of fruit development has been central in the evolution and domestication of flowering plants. In common bean (Phaseolus vulgaris L.), a major global staple crop, the two main economic categories are distinguished by differences in fiber deposition in pods: a) dry beans with fibrous and stringy pods; and b) stringless snap/green beans with reduced fiber deposition, but which frequently revert to the ancestral stringy state. To better understand control of this important trait, we first characterized developmental patterns of gene expression in four phenotypically diverse varieties. Then, using isogenic stringless/revertant pairs of six snap bean varieties, we identified strong overexpression of the common bean ortholog of INDEHISCENT (PvIND) in non-stringy types compared to their string-producing counterparts. Microscopy of these pairs indicates that PvIND overexpression is associated with overspecification of weak dehiscence zone cells throughout the entire pod vascular sheath. No differences in PvIND DNA methylation were correlated with pod string phenotype. Sequencing of a 500 kb region surrounding PvIND in the stringless snap bean cultivar Hystyle revealed that PvIND had been duplicated into two tandem repeats, and that a Ty1-copia retrotransposon was inserted between these tandem repeats, possibly driving PvIND overexpression. Further sequencing of stringless/revertant isogenic pairs and diverse materials indicated that these sequence features had been uniformly lost in revertant types and were strongly predictive of pod phenotype, supporting their role in PvIND overexpression and pod string phenotype. SignificanceFruit dehiscence is a key trait for seed dissemination. In legumes, e.g., common bean, dehiscence relies on the presence of fibers, including pod "strings". Selections during domestication and improvement have decreased (dry beans) or eliminated (snap beans) fibers, but reversion to the fibrous state occurs frequently in snap beans. In this article, we document that fiber loss or gain is controlled by structural changes at the PvIND locus, a homolog of the Arabidopsis INDEHISCENT gene. These changes include a duplication of the locus and insertion/deletion of a retrotransposon, which are associated with significant changes in PvIND expression. Our findings shed light on the molecular basis of unstable mutations and provide potential solutions to an important pod quality issue. Competing Interest StatementThe authors have no competing interests.