Auxin apical dominance governed by the OsAsp1-OsTIF1 complex determines distinctive rice caryopses development on different branches

Abstract

In rice ( Oryza sativa), caryopses located on proximal secondary branches (CSBs) have smaller grain size and poorer grain filling than those located on apical primary branches (CPBs), greatly limiting grain yield. However, the molecular mechanism responsible for developmental differences between CPBs and CSBs remains elusive. In this transcriptome-wide expression study, we identified the gene Aspartic Protease 1 ( OsAsp1), which reaches an earlier and higher transcriptional peak in CPBs than in CSBs after pollination. Disruption of OsAsp1 expression in the heterozygous T-DNA line asp1-1 ^+/–eliminated developmental differences between CPBs and CSBs. OsAsp1 negatively regulated the transcriptional inhibitor of auxin biosynthesis, Os T AA1 transcriptional inhibition factor 1 (OsTIF1), to preserve indole-3-acetic acid (IAA) apical dominance in CPBs and CSBs. IAA also facilitated OsTIF1 translocation from the endoplasmic reticulum (ER) to the nucleus by releasing the interaction of OsTIF1 with OsAsp1 to regulate caryopses IAA levels via a feedback loop. IAA promoted transcription of OsAsp1 through MADS29 to maintain an OsAsp1 differential between CPBs and CSBs during pollination. Together, these findings provide a mechanistic explanation for the distributed auxin differential between CPBs and CSBs to regulate distinct caryopses development in different rice branches and potential targets for engineering yield improvement in crops.

Author summary

Rice is a major food crop and an important model plant. Compared with caryopses on apical primary branches (CPBs) of rice, those located on proximal secondary branches (CSBs) display smaller grains and poor grain filling, which greatly limit rice yield potential fulfilment, especially among ‘super’ rice cultivars. In this study, we demonstrated that high indole-3-acetic (IAA) levels upregulated Aspartic Protease 1 ( OsAsp1) transcription via MADS29 post-pollination to produce higher OsAsp1 levels in CPBs than in CSBs. OsAsp1 then interacted with Os T AA1 transcriptional inhibition factor 1 (OsTIF1) in the endoplasmic reticulum (ER) to dispel OsTIF1 transcriptional inhibition of OsTAA1, causing IAA content to peak in CPBs at 5 days after fertilisation (DAF). IAA facilitated OsTIF1 translocation from the ER to the nucleus by reducing its interaction with OsAsp1 as feedback regulation of IAA levels in caryopses. Thus, differential auxin levels between CPBs and CSBs are determined by the OsAsp1-OsTIF1 complex, and are essential for the distinct development of CPBs and CSBs, providing potential targets for engineering yield improvement in crops.