A mutation in a C2H2-type zinc finger transcription factor contributed to the transition toward self-pollination in cultivated tomato

Abstract

The degree of stigma exsertion has a major influence on self-pollination efficiency in tomato, and its improvement is essential for raising productivity and for fixing advantageous traits in cultivated tomato. To study the evolution of stigma exsertion degree in tomato, we searched for genes associated with this trait and other aspects of flower morphology, including the lengths of anthers, styles, and ovaries. We performed a genome-wide association on 277 tomato accessions and discovered a novel stigma exsertion gene (SE3.1). We reannotated the structure of the gene, which encodes a C2H2-type zinc finger transcription factor. A mutation of the lead SNP creates a premature termination codon in SE3.1 and an inserted stigma in cultivated tomatoes. SE3.1 is essential for the conversion of flush stigmas to inserted stigmas. This conversion has a major impact on the rate of self-fertilization. Intriguingly, we found that both SE3.1 and Style2.1 contribute to the transition from stigma exsertion to insertion during the domestication and improvement of tomato. Style2.1 controls the first step of exserted stigmas to flush stigmas, and SE3.1 controls the second step of flush stigmas to inserted stigmas. We provide molecular details for the two-step process that controls the transition from stigma exsertion to insertion, which is of great agronomic importance in tomato.

Variation in the fruit development gene POINTED TIP regulates protuberance of tomato fruit tip

“…To determine whether PT could have been a target of selection in the process of tomato domestication and improvement, we evaluated the nucleotide diversity (π) between groups that we previously evaluated 30 . Comparing the ratios of nucleotide diversity between PIM and CER accessions, we found that PT was part of a large genomic cluster with a high ratio of diversity, indicating one or several selection events during tomato domestication (Fig.…”

“…In Arabidopsis , KNUCKLES ( KNU ) might function as a transcriptional repressor of cellular proliferation that regulates floral determinacy and basal pattern elements because the knu mutant develops flowers and siliques with abnormal morphologies 26 . Previous studies have predicted 112 C2H2-type transcription factors in tomato 27 , and they have been implicated in multiple processes, such as ZF3 in salt tolerance 28 , Hair in trichome formation 29 , SE3.1 in flower development 30 , OBV in leaf veins development 31 . However, the natural variation of C2H2 zinc finger proteins and their influence on fruit shape in natural populations remains largely unknown.…”

Fine mapping and target gene identification of qSE4, a QTL for stigma exsertion rate in rice (Oryza sativa L.)

“…SE3.1 controls stigma exsertion, which is not related to its expression level but is related to its gene function. The loss of SE3.1 function promotes tomato stigma retraction, while Style2.1 and SE3.1 are key genes that regulate the two-step process of stigma from exsertion to insert during tomato domestication ( Shang et al, 2021 ). Recently, there was a major breakthrough in the study of stigma exsertion in legumes.…”

The selfing syndrome and beyond: diverse evolutionary consequences of mating system transitions in plants

“…Downregulation of Style2.1 owing to a 450 bp deletion in the promoter region was responsible for reduced anther–stigma separation in domesticated tomatoes. Recently, another stigma exsertion gene ( SE3.1 ) was also identified through a GWAS in a population of 277 tomato accessions [25]. A loss-of-function mutation in the SE3.1 gene was shown to create an inserted stigma, having a major impact on the selfing rate.…”