Calcium signalling mediates self-incompatibility response in the Brassicaceae

Abstract

Self-incompatibility in the Brassicaceae is controlled by multiple haplotypes encoding the pollen ligand (S-locus protein 11, SP11, also known as S-locus cysteine-rich protein, SCR) and its stigmatic receptor (S-receptor kinase, SRK). A haplotype-specific interaction between SP11/SCR and SRK triggers the self-incompatibility response that leads to self-pollen rejection, but the signalling pathway remains largely unknown. Here we show that Ca(2+) influx into stigma papilla cells mediates self-incompatibility signalling. Using self-incompatible Arabidopsis thaliana expressing SP11/SCR and SRK, we found that self-pollination specifically induced an increase in cytoplasmic Ca(2+) ([Ca(2+)]cyt) in papilla cells. Direct application of SP11/SCR to the papilla cell protoplasts induced Ca(2+) increase, which was inhibited by D-(-)-2-amino-5-phosphonopentanoic acid (AP-5), a glutamate receptor channel blocker. An artificial increase in [Ca(2+)]cyt in papilla cells arrested wild-type (WT) pollen hydration. Treatment of papilla cells with AP-5 interfered with self-incompatibility, and Ca(2+) increase on the self-incompatibility response was reduced in the glutamate receptor-like channel (GLR) gene mutants. These results suggest that Ca(2+) influx mediated by GLR is the essential self-incompatibility response leading to self-pollen rejection.

Advances and current challenges in calcium signaling

“…A final [Ca 2+ ] cyt transient was observed after successful fertilization (Iwano et al ., ; Denninger et al ., ; Hamamura et al ., ; Ngo et al ., ). Ca 2+ signals, likely mediated by glutamate receptor‐like channels appeared to be important for the self‐incompatibility response (Iwano et al ., ). The sperm delivery process during double fertilization appeared to be coordinated by the FERONIA signaling pathway (Ngo et al ., ).…”

“…Here, Ca 2+ signals in pollen tubes were visualized using R-GECO1, whereas synergid Ca 2+ concentrations were monitored using YC3.6 (Ngo et al, 2014) (Iwano et al, 2012;Denninger et al, 2014;Hamamura et al, 2014;Ngo et al, 2014). Ca 2+ signals, likely mediated by glutamate receptor-like channels appeared to be important for the self-incompatibility response (Iwano et al, 2015). The sperm delivery process during double fertilization appeared to be coordinated by the FERONIA signaling pathway (Ngo et al, 2014).…”

Pollen-Pistil Interactions and Their Role in Mate Selection

“…and Arabidopsis, the SCR protein diffuses from the pollen exine and interacts with the SRK extracellular domain, which is located in the plasma membrane of the stigmatic papillar cells. SRK signals to intracellular proteins in the papillar cell, and downstream events, including protein phosphorylation and changes in intracellular calcium, lead to the rejection response (Takayama and Isogai, 2005;Nasrallah and Nasrallah, 2014;Iwano et al, 2015). In compatible pollinations, independent of SRK signaling, the papillar cells are stimulated to secrete material that presumably supports pollen tube growth (Safavian and Goring, 2013).…”

Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition

“…Identification of the pattern-triggered calcium channel remains a challenging task, but several plasma membrane-localized calcium permeable channels such as GLUTAMATE-LIKE RECEPTORs (GLRs), CYCLIC NUCLEOTIDE GATED CHANNELs (CNGCs), and REDUCED HYPEROSMOLARITY-INDUCED [Ca 2+ ] i INCREASEs (OSCAs) exist in plants (Dodd et al, 2010;Hou et al, 2014;Yuan et al, 2014). For instance, GLRs are required for [Ca 2+ ] cyt increase in the pollen tube during self-incompatibility (Iwano et al, 2015). OSCA1 is required for ([Ca 2+ ] cyt ) increase during osmotic stress (Hou et al, 2014;Yuan et al, 2014).…”