Molecular characteristics of S-RNase alleles as the determinant of self-incompatibility in the style of Fragaria viridis

Jianke Du,Yushan Qiao,Sanhong Wang,Tingting Li,Chunfeng Ge,Zhihong Gao,Hidenori Sassa

doi:10.1038/s41438-021-00623-x

Jianke Du, Yushan Qiao + Show 5 more

Open Access

https://doi.org/10.1038/s41438-021-00623-x

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Abstract

Strawberry (Fragaria spp.) is a member of the Rosoideae subfamily in the family Rosaceae. The self-incompatibility (SI) of some diploid species is a key agronomic trait that acts as a basic pollination barrier; however, the genetic mechanism underlying SI control in strawberry remains unclear. Two candidate S-RNases (Sa- and Sb-RNase) identified in the transcriptome of the styles of the self-incompatible Fragaria viridis 42 were confirmed to be SI determinants at the S locus following genotype identification and intraspecific hybridization using selfing progenies. Whole-genome collinearity and RNase T2 family analysis revealed that only an S locus exists in Fragaria; however, none of the compatible species contained S-RNase. Although the results of interspecific hybridization experiments showed that F. viridis (SI) styles could accept pollen from F. mandshurica (self-compatible), the reciprocal cross was incompatible. Sa and Sb-RNase contain large introns, and their noncoding sequences (promotors and introns) can be transcribed into long noncoding RNAs (lncRNAs). Overall, the genus Fragaria exhibits S-RNase-based gametophytic SI, and S-RNase loss occurs at the S locus of compatible germplasms. In addition, a type of SI-independent unilateral incompatibility exists between compatible and incompatible Fragaria species. Furthermore, the large introns and neighboring lncRNAs in S-RNase in Fragaria could offer clues about S-RNase expression strategies.

Highlights

The germplasm of low ploidy wild strawberry contains abundant genetic resources that control valuable traits and is a potential resource for improving cultivated strawberry
The phenotype is determined by the S haplotype of the pollen, which results in the generation of samegenotype pollen tubes that cannot normally extend to the ovary in the style[9]; this process may involve multiple genetic mechanisms
In contrast to non-S-RNase genes, S-RNase, as a candidate SI determinant, has specific characteristics that distinguish it from other RNase genes[11,15,18]

Summary

Introduction

The germplasm of low ploidy wild strawberry contains abundant genetic resources that control valuable traits and is a potential resource for improving cultivated strawberry. Pollination obstacles between styles and pollen have considerably hampered strawberry breeding[1,2,3,4,5,6]. Incompatibility includes self-incompatibility (SI) and interspecific incompatibility, and it has been demonstrated that both have common genetic factors and share some intermediate mechanisms in Solanaceae[7,8]. Gametophytic SI (GSI) is a genetic mechanism that inhibits the self-pollination and growth of inbred pollen tubes. Two GSI mechanisms have been identified, including S-RNase-based GSI, identified in Solanaceae, Plantaginaceae, and Rosaceae, and signal transduction GSI, identified in Papaveraceae[7,10,11]. Strawberries belong to the genus Fragaria in the subfamily Rosoideae (family Rosaceae).

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