In the mustard family, which includes the important crop Brassica (rapeseed/canola) and the model plant Arabidopsis, the surfaces of the female stigmatic cells are dry. These cells – on which the pollen grains land – are thought to be more advanced than those of the wet stigmas of many other plants because they do not trap fungal spores (or pollen grains of many other species), and can discriminate between self and cross pollen of their own species and thus avoid self-pollination. The evolution of these stigmas has, however, involved the development of a good deal of complex cell biology – primarily to enable their own pollen to adhere to the dry surface, and to hydrate, germinate and penetrate the stigmatic cuticle.
The molecular interactions underpinning this so-called basal compatibility response (BCR) are currently being unraveled in Daphne Goring’s laboratory at the University of Toronto. In presenting the 2015 Annals of Botany Special Lecture at Oxford University’s Department of Plant Sciences on June 15th, Professor Goring described her most recent work on the signaling pathways regulating the BCR in Brassica and Arabidopsis species, and explained how these systems are linked to the genetically-based system of self-incompatibility that prevents self-pollen development on the stigma surface (See figure below for summary).
Her talk focused on the different signaling components that regulate the stigmatic papillar (hair) cell responses to compatible (out-crossing) pollen and self (incompatible) pollen (reviewed in Indriolo et al., 2014). In response to challenge by compatible pollen, the BCR signalling pathway is activated in the stigmatic cytoplasm below the point of pollen contact, which leads to vesicle secretion in Arabidopsis species, and secretion by multivesicular bodies (MVBs) in Brassica species (Elleman and Dickinson, 1990, 1996; Safavian and Goring, 2013; Indriolo et al., 2014). This polarized secretion under the pollen/stigma contact site is mediated by components of the exocyst complex (Samuel et al., 2009; Safavian et al., 2015) which are known to tether vesicles to specific ‘target’ membranes for fusion and the release of their cargo (reviewed in Zarsky et al., 2013). Professor Goring suggested that this cargo facilitates pollen hydration, germination and pollen tube entry into the stigma. Although the identity of this cargos is unknown, one promising candidate is the ACA13 Ca2+-ATPase – proposed to release Cas
Professor Goring then described how the BCR signalling pathway is also initiated in response to self-incompatible pollen, leading again to vesicle/MVB formation in the cytoplasm. However, in Arabidopsis species she showed new data suggesting that autophagy is then induced, resulting in the inhibition of exocytosis and destruction of cytoplasmic material – including secretory vesicles. In Brassica, exocytosis also fails to occur for MVBs are rerouted to the vacuole for degradation (Safavian and Goring, 2013; Indriolo et al., 2014). It has been known for some time that this self-incompatibility cellular response is initiated by a polymorphic pollen ligand (SP11/SCR) and a polymorphic stigma S Receptor Kinase (SRK; reviewed in Iwano and Takayama, 2012). Professor Goring described recent experiments showing how the ARC1 E3 ubiquitin ligase functions downstream of SRK in this self-incompatibility signalling pathway and may act to inhibit an exocyst subunit, Exo70A1, to prevent exocytosis (Stone et al., 1999; Stone et al., 2003; Samuel et al., 2009; Indriolo et al., 2012; Indriolo et al., 2014). Her experimental data also show that ARC1 is linked to the autophagy response, but precisely how autophagy is initiated in the self-incompatibility pathway is as yet unclear (reviewed in Goring et al., 2014). Of course, by blocking exocytosis, the cargo needed for pollen ‘acceptance’ remains undelivered, and self-incompatible pollen is thus rejected, being unable to hydrate and/or germinate.
Pollination systems of this type are emerging as important paradigms for cell-cell signalling in plants. Furthermore, understanding how pollen is accepted and rejected on dry stigmatic surfaces will also be essential for the development of new plant breeding strategies for brassica crops, and may even help identify mechanisms by which plants recognise and reject fungal pathogens.
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