Abstract
Self-incompatibility (SI) is a genetic mechanism flowering plants adopted to reject self-pollen and promote outcrossing. In the Brassicaceae family plants, the stigma tissue plays a key role in self-pollen recognition and rejection. We reported earlier in Chinese cabbage (Brassica rapa) that stigma tissue showed upregulated ethylene responses and programmed cell death (PCD) upon compatible pollination, but not in SI responses. Here, we show that SI is significantly compromised or completely lost in senescent flowers and young flowers of senescent plants. Senescence upregulates senescence-associated genes in B. rapa. Suppressing their expression in young stigmas by antisense oligodeoxyribonucleotide abolishes compatible pollination-triggered PCD and inhibits the growth of compatible pollen tubes. Furthermore, ethylene biosynthesis genes and response genes are upregulated in senescent stigmas, and increasing the level of ethylene or inhibiting its response increases or decreases the expression of senescence-associated genes, respectively. Our results show that senescence causes PCD in stigmatic papilla cells and is associated with the breakdown of SI in Chinese cabbage and in radish.
Highlights
Self-incompatibility (SI) is a genetic mechanism widely adopted by flowering plants and present in roughly half of the species to promote outcrossing and prevent inbreeding (de Nettancourt, 1977)
We showed that treating stigmas with ethephon, an ethylene-releasing reagent, induces programmed cell death (PCD) in the stigmatic papilla cells and breaks down SI in heading Chinese cabbage (Su et al, 2020)
In field and greenhouse experiments, flowers from Brassica family plants senesce within 1 day after cross-pollination, whereas flowers that have not been pollinated by compatible pollen last 2–5 days on the inflorescence even after they pass the prime pollination stage
Summary
Self-incompatibility (SI) is a genetic mechanism widely adopted by flowering plants and present in roughly half of the species to promote outcrossing and prevent inbreeding (de Nettancourt, 1977). As the Brassicaceae have dry stigmas, only compatible pollen grains are capable of inducing the stigma to release necessary resources, such as water and other factors, but the absence of surface secretions prevents SI pollen or unrelated foreign pollen from adhering, hydrating, and germinating at the earliest stages of pollination (Samuel et al, 2009; Jany et al, 2019). Brassicaceae SI is controlled by two genetically linked polymorphic S loci: the pollen-coat-expressed S-locus cysteinerich protein (SP11/SCR) and the stigma-specific S-locus Ser/Thr receptor kinase (SRK) (Nasrallah, 2019). Subsequent intracellular signaling pathways in the papilla cells lead to the rejection of self-pollen either by blocking hydration and germination of pollen or by restricting pollen tube growth into the stigma (Samuel et al, 2009; Indriolo et al, 2012; Sankaranarayanan et al, 2015, 2017; Scandola and Samuel, 2019; Jany et al, 2019)
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