Transcriptome and phytohormone analysis reveals a comprehensive phytohormone and pathogen defence response in pear self-/cross-pollination

Abstract

Key message Candidate genes were identified and the role of phytohormones such as JA-Me and ABA in the synthesis of S-RNase was emphasized in pear selfincompatibility. Abstract Self-incompatibility (SI) occurs widely in flowering plants as an intraspecific reproductive barrier. This phenomenon promotes variation within species, but for some species such as Pyrus, SI is a nuisance rather than a benefit in agricultural production. Although many studies have been conducted on SI in pears, its mechanism remains unclear. In this study, high-throughput Illumina RNA sequencing (RNA-seq) was used to identify SI-related genes in pear styles. Using transcriptome comparisons, differentially expressed genes of unpollinated (UP), crosspollinated (CP), and self-pollinated (SP) styles were identified after 48 h. A total of 1796 and 1890 genes were identified in DSC (UP vs. CP) and DSI (UP vs. SP), respectively. KEGG analysis revealed that genes involved in the ''plant hormone signal transduction pathway'' and ''plant-pathogen interaction pathway'' were significantly enriched in DSI (UP vs. SP) compared to those in DSC (UP vs. CP). The expression level of S-glycoprotein ribonuclease (S-RNase) was dramatically reduced in cross-pollinated (CP) styles. To better understand the relationship between the expression patterns of S-RNase and two major KEGG pathways, the concentrations of phytohormones were measured, and the expression pattern of S-RNase was analysed using qRT-PCR. Our results demonstrate that methyl jasmonate and abscisic acid may enhance the expression level of S-RNase, and pollination can affect the synthesis of methyl jasmonate and abscisic acid in pear styles. Overall, this study is a global transcriptome analysis of SI in pear. A relationship between self-rejection, plant hormones, and pathogen defence was shown in pear.Keywords Pear (Pyrus bretschneideri Rehd.) Á Selfincompatibility Á Transcriptome Á S-RNase Á Methyl jasmonate

In-Depth Understanding of Camellia oleifera Self-Incompatibility by Comparative Transcriptome, Proteome and Metabolome

“…This suggested that plant hormones might work together to regulate plant cell PCD. DETs after selfand cross-pollination were significantly enriched in plant hormone signal transduction pathway and plant-pathogen interaction pathway using transcriptomics in pears [22]. Likewise, it also demonstrated that jasmonate (JA) and abscisic acid (ABA) might enhance the expression level of S-RNase, which caused the PCD of the pollen tube in SI.…”

“…Hormone signal transduction and MAPKs are associated with responses to SI [22,29,30]. A previous study provided evidence that MAPKs could induce PCD [41][42][43].…”

“…S-RNase can affect the degradation of pollen tube RNA and depolymerize the cytoskeleton, resulting in the occurrence of programmed cell death (PCD) in the pollen tube in Pyrus bretschneideri [21]. As S-RNase possesses cytotoxicity, it seems that S-RNase may trigger signaling pathways or defense responses following its entry into the pollen tube [21][22][23]. Contrary to the GSI and SSI systems where self-pollination pollen is stopped before reaching the ovary, a self-pollination pollen tube in LSI can grow smoothly in the style and reach the ovary, but in the end, it cannot be seeded or the seed-setting rate is significantly lower than that of the cross-pollinated plants [8].…”

RNA-Seq analysis of compatible and incompatible styles of Pyrus species at the beginning of pollination

“…The transcription rate of genes for pathogenesis-related proteins was increased in only 5 min during the HP response (Hiscock & Mcinnis, 2004). In a previous study, after 48 h of pollination, the gene expression of pear ( P. bretschneideri ) was compared in the style, and it was speculated that the plants could identify compatible and incompatible pollen using the plant-pathogen signaling system at the start of pollination (Shi et al , 2017). Therefore, we believe that the mutual recognition of the pollen and stigma in GSI of Rosaceae is similar to the pollen and stigma recognition process in the sporophytic self-incompatibility of Brassica spp.…”

A gamma‐thionin protein from apple, MdD1, is required for defence against S‐RNase‐induced inhibition of pollen tube prior to self/non‐self recognition

“…Consistent with these results, a study by Shi et al . () on S ‐RNase‐based SI in pear found that expression of genes involved in the ‘plant hormone signal transduction pathway’ and ‘plant–pathogen interaction pathway’ was significantly enriched in self‐ and cross‐pollinations (Shi et al ., ). Furthermore, previous reports have indicated that MYC2 can bind G‐box‐related motifs (Gangappa and Chattopadhyay, ; Kazan and John, ), and in this study, we identified a new signalling component, MdD1 , using a ChIP‐seq approach (Figure ).…”