Abstract
The inhibition of self-pollination in self-incompatible Brassicaceae is based on allele-specific trans-activation of the highly polymorphic S-locus receptor kinase (SRK), which is displayed at the surface of stigma epidermal cells, by its even more polymorphic pollen coat-localized ligand, the S-locus cysteine-rich (SCR) protein. In an attempt to achieve constitutive activation of SRK and thus facilitate analysis of self-incompatibility (SI) signaling, we coexpressed an Arabidopsis lyrata SCR variant with its cognate SRK receptor in the stigma epidermal cells of Arabidopsis (Arabidopsis thaliana) plants belonging to the C24 accession, in which expression of SRK and SCR had been shown to exhibit a robust SI response. Contrary to expectation, however, coexpression of SRK and SCR was found to inhibit SRK-mediated signaling and to disrupt the SI response. This phenomenon, called cis-inhibition, is well documented in metazoans but has not as yet been reported for plant receptor kinases. We demonstrate that cis-inhibition of SRK, like its trans-activation, is based on allele-specific interaction between receptor and ligand. We also show that stigma-expressed SCR causes entrapment of its SRK receptor in the endoplasmic reticulum, thus disrupting the proper targeting of SRK to the plasma membrane, where the receptor would be available for productive interaction with its pollen coat-derived SCR ligand. Although based on an artificial cis-inhibition system, the results suggest novel strategies of pollination control for the generation of hybrid cultivars and large-scale seed production from hybrid plants in Brassicaceae seed crops and, more generally, for inhibiting cell surface receptor function and manipulating signaling pathways in plants.
Highlights
The inhibition of self-pollination in self-incompatible Brassicaceae is based on allele-specific trans-activation of the highly polymorphic S-locus receptor kinase (SRK), which is displayed at the surface of stigma epidermal cells, by its even more polymorphic pollen coat-localized ligand, the S-locus cysteine-rich (SCR) protein
To coexpress an SRK variant with its cognate SCR in stigma epidermal cells, we used the SRKb and SCRb alleles, which are derived from the A. lyrata S-locus haplotype b (Sb) haplotype (Kusaba et al, 2001), and the C24 accession of Arabidopsis, which was previously shown to exhibit a robust and developmentally SI response upon transformation with the SRKb-SCRb gene pair (Nasrallah et al, 2004; Boggs et al, 2009; Nasrallah and Nasrallah, 2014b)
The SRK/SCR-mediated signaling that occurs upon contact between a stigma epidermal cell and a pollen grain conforms to the classical view of cell contactdependent receptor-based cell-to-cell signaling, in which the directionality of signaling is defined by expression of a receptor in the signal-receiving cell and of its cognate ligand in a signal-sending adjacent cell
Summary
The inhibition of self-pollination in self-incompatible Brassicaceae is based on allele-specific trans-activation of the highly polymorphic S-locus receptor kinase (SRK), which is displayed at the surface of stigma epidermal cells, by its even more polymorphic pollen coat-localized ligand, the S-locus cysteine-rich (SCR) protein. This communication typically relies on the interaction of transmembrane receptors displayed on the surface of signal-receiving cells with their cognate ligands derived from signal-sending neighboring cells, which, in turn, leads to the activation of receptor-mediated signaling cascades that modify intracellular activities of the signalreceiving cell Such is the case with communication between pollen grains and stigma epidermal cells, a process that has an important role in directing reproductive success and determining pollination modes (i.e. selfing or outcrossing) in the Brassicaceae. Constitutive activation of receptor kinases has been shown to result from receptor mutations that cause constitutive kinase activity (Webster and Donoghue, 1996; Hirota et al, 1998) and mutations in signaling components that cause ligandindependent activation of downstream cascades (Wang et al, 2012, 2014; Roberts et al, 2013; Han, 2014), and from ectopic expression of ligands within the same cells as their receptors, as occurs in several pathological conditions (Sporn and Roberts, 1985; Castellano et al, 2006; Krasagakis et al, 2011)
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