Late-acting self-incompatibility (LSI) in Schima superba: pollen-ovary interactions and signaling to trigger PCD in incompatible pollen

Background: In angiosperm, Self-incompatibility (SI) is a common and widespread mechanism for plant preventing inbreeding risk and late-acting self-incompatibility (LSI) is even more ancestral conserved. In this work, we worked on Schima superba , one species in Theaceae, commercially important timer and fire-resistant tree species and revealed its LSI mechanism. Results The self-pollen tubes grew to the bottom of the stylus and enter ovary until 48h, but failed to penetrate the ovule. Meanwhile, the hormone and peroxidase levels were dramatically changed. Transcriptome and proteome analysis explored the molecular mechanisms of LSI and candidate genes related to LSI in S.superba . Overall 586.71 million reads were obtained and 79,642 (39.08%) unigenes were annotated. KEGG and GO showed that 4531 differentially expressed genes (DEGs) and 82 differentially expressed proteins (DEPs) were at 48h in self- (SP) vs outcross-pollination (OP). Among these, 160 DEGs and 33 DEPs involved in pollen-pistil interaction. The “pollen-pistil interaction”, “signal recognition” and “component of membrane” were downregulated in SP whereas the “cell wall and membrane biosynthetic process”, “oxidoreductase activity” were upregulated. The DEGs involved with S-RNases and SCF during SP suggested that the LSI was happened at 48h ovary, and the LSI in S.superba was under gametophyte control. The calcium ion increase-releasement and F-actin depolymerization initiated metacaspases-1 activity and lead to PCD progress. Also, mitochondrial function loss and ROS disruption further aggravated the PCD progress and cell death. Cell wall biosynthetic progress upregulated and cellulose synthase downregulated could lead to ovary xylification and withering. Conclusions The LSI of S.superba which happened at 48h after pollination was key time point. The incompatibility PT ceased growth in ovary because of the S-RNase recognition and PCD happened in this organ. This study highlight the LSI molecular mechanism in S.superba and also gave a reference to other species in Theaceae.