Exploring the Loci Responsible for Awn Development in Rice through Comparative Analysis of All AA Genome Species

Abstract

Wild rice species have long awns at their seed tips, but this trait has been lost through rice domestication. Awn loss mitigates harvest and seed storage; further, awnlessness increases the grain number and, subsequently, improves grain yield in Asian cultivated rice, highlighting the contribution of the loss of awn to modern rice agriculture. Therefore, identifying the genes regulating awn development would facilitate the elucidation of a part of the domestication process in rice and increase our understanding of the complex mechanism in awn morphogenesis. To identify the novel loci regulating awn development and understand the conservation of genes in other wild rice relatives belonging to the AA genome group, we analyzed the chromosome segment substitution lines (CSSL). In this study, we compared a number of CSSL sets derived by crossing wild rice species in the AA genome group with the cultivated species Oryza sativa ssp. japonica. Two loci on chromosomes 7 and 11 were newly discovered to be responsible for awn development. We also found wild relatives that were used as donor parents of the CSSLs carrying the functional alleles responsible for awn elongation, REGULATOR OF AWN ELONGATION 1 (RAE1) and RAE2. To understand the conserveness of RAE1 and RAE2 in wild rice relatives, we analyzed RAE1 and RAE2 sequences of 175 accessions among diverse AA genome species retrieved from the sequence read archive (SRA) database. Comparative sequence analysis demonstrated that most wild rice AA genome species maintained functional RAE1 and RAE2, whereas most Asian rice cultivars have lost either or both functions. In addition, some different loss-of-function alleles of RAE1 and RAE2 were found in Asian cultivated species. These findings suggest that different combinations of dysfunctional alleles of RAE1 and RAE2 were selected after the speciation of O. sativa, and that two-step loss of function in RAE1 and RAE2 contributed to awnlessness in Asian cultivated rice.

DOMINANT AWN INHIBITOREncodes the ALOG Protein Originating from Gene Duplication and Inhibits AWN Elongation by Suppressing Cell Proliferation and Elongation in Sorghum

“…Extensive studies of awn formation and elongation in rice revealed that awnless cultivars were established by sequentially selecting loss-of-function alleles or genes involved in awn formation and elongation during domestication (Amarasinghe et al 2020, Bessho-Uehara et al 2021). An-1 [also known as REGULATOR OF AWN ELONGATION 1 (RAE1); hereinafter referred to as An-1/RAE1] encodes a basic helix-loop-helix transcription factor expressed at the apex of the lemma primordia, which causes continuous cell division for awn elongation (Luo et al 2013, Furuta et al 2015.…”

Characterization of Domestication Loci Associated with Awn Development in Rice

“…qAwn2.2 is located close to qAWNL2 and An-4 (Amarasinghe et al 2020 ; Qin et al 2021 ). qAwn11.1 overlapped with an awn QTL on chromosome 11 (Bessho-Uehara et al, 2021 ). These co-locations of the known genes/QTLs detected in previous studies could provide proof of the accuracy of our analysis.…”

“…Some minor QTLs, qAWNL2 and An-4 , have also been detected using populations derived from interspecific crosses (Amarasinghe et al 2020 ; Qin et al 2021 ). Recently, a study explored the loci responsible for awn development in rice through a comparative analysis of all AA genome species (Bessho-Uehara et al 2021 ). Most known genes/QTLs for awn development were also detected, and two loci on chromosomes 7 and 11 were newly identified in that study.…”

“…Considerable interest exists in discovering genes and genetic mechanisms contributing to awn reduction during domestication because it may facilitate basic research and trait manipulation through breeding strategies (Bessho-Uehara et al 2021 ; Ross-Ibarra et al 2007 ). Moreover, rice domestication initially resulted from selection on natural mutations in wild rice.…”

“…Recently, studies have been conducted to elucidate the genetic mechanisms underlying the development of rice awns. These results suggest that awn development is a complex trait regulated by many genes and is mostly observed in wild rice (Bessho-Uehara et al 2021;Amarasinghe et al 2020;Qin et al 2021;Wang et al 2011). Although several awn-related quantitative trait loci (QTLs) have been detected, only a few major QTLs have been cloned and characterized at the molecular level.…”