Self‐Incompatibility

Abstract

Complex pollen–pistil (male–female) interactions play a decisive role in determining reproductive success following pollination. Self‐incompatibility (SI) is a genetically controlled mechanism to prevent self‐fertilisation, ensuring genetic diversity of offspring. Three SI systems have been well characterised at a molecular/cellular level; they utilise highly polymorphic, tightly linked pollen‐ and pistil‐expressed S ‐determinants. All three characterised SI systems have different S‐determinants and employ contrasting mechanisms to reject incompatible pollen. The Brassica and Papaver SI system operate using self‐recognition, while the S‐RNase SI system employs self‐/non‐self recognition. In Brassica , a receptor‐kinase ligand interaction, together with modifiers involving a ubiquitin degradation pathway which suppresses compatibility factors, results in the rejection of incompatible pollen. The Papaver SI system utilises a receptor–ligand type interaction that triggers a calcium‐dependent signalling network culminating in the programmed cell death of incompatible pollen. In the S‐RNase SI system, some form of detoxification of the ribonuclease activity takes place in compatible pollen tubes. Key Concepts Pollen–pistil interactions are pivotal in determining the reproductive outcomes in flowering plants. Self‐incompatibility (SI) is an important mechanism used by many flowering plants to prevent self‐fertilisation as enforced outcrossing ensures increased heterozygosity and this prevention of self‐seed set helps maintain genetic diversity and fitness. Self‐incompatibility loci are highly polymorphic and as many as 60 S ‐alleles are present at a single S ‐locus; this is comparable to the major histocompatibility complex in animals that allows self‐/non‐self discrimination by T cells. Three mechanistically distinct SI systems have been identified and as they employ different S‐determinants and mechanisms to prevent self‐fertilisation, this suggests that SI evolved independently at least three times, and probably many more times. In the Brassica SI system, the male S‐determinant is SCR/SP11, a small cysteine‐rich protein in the pollen coat, and the female S‐determinant, SRK, is a receptor kinase. In Brassica, following a ‘self’ pollen–stigma interaction, SCR/SP11 binds and activates SRK, triggering an intracellular signalling cascade in the stigma that suppress compatibility factors, resulting in the rejection of incompatible pollen In the Papaver SI system, the female S‐determinant, PrsS, is a small cysteine‐rich protein secreted by the stigma and the male S‐determinant is PrpS, a novel transmembrane protein. In Papaver, following a ‘self’ pollen–stigma interaction, a receptor–ligand type interaction between PrpS and PrsS takes place, triggering a calcium‐dependent signalling network culminating in the triggering of programmed cell death in incompatible pollen. In the S‐RNase SI system, the female S‐determinant is a ribonuclease: S‐RNase and the male S‐determinants are F‐box proteins. There are two conflicting models for how the S‐RNase SI system operates: both involve some form of detoxification of the S‐RNases in compatible pollen tubes, using either degradation by a ubiquitin pathway or compartmentalisation and selective release. Knowledge about the molecular basis of SI may provide opportunities for translational science and using SI for crop improvement may provide useful applications, for example to breed hybrid crops.

The Nβ motif of NaTrxh directs secretion as an endoplasmic reticulum transit peptide and variations might result in different cellular targeting

“…NaTrxh is directly involved in Nicotiana ’s gametophytic SI system, known as S-RNase-dependent SI [ 18 ]. SI is a genetically controlled system that acts as a barrier to self-pollination and involves complex pollen-pistil interactions in which secreted stylar proteins play key roles [ 19 – 21 , 52 , 53 ]. The S-RNase–the female S determinant–and NaTrxh colocalise to the extracellular matrix of the stylar transmitting tissue in N .…”

“…In vitro NaTrxh interacts with and reduces the S-RNase protein [ 15 , 17 , 18 ], which is a secretory protein of the stylar transmitting tissue and is the female S-determinant of the S-RNase-based self-incompatibility (SI) system (rev. within [ 19 – 21 ]). S-RNase reduction by NaTrxh results in a seven-fold increase in ribonuclease activity that is essential for self-pollen rejection in Nicotiana [ 18 ].…”

Pre-zygotic mate selection affects progeny fitness and is only partially correlated with the expression ofNaS-like RNases

“…Flowering plants have evolved a variety of different mating systems that differ in mechanism and pollen preference (Pannell & Voillemot, 2017; Whitehead et al ., 2018). One of the best characterized examples is the rejection of self pollen in self-incompatible (SI) species, ensuring the genetic diversity of the progeny (Muñoz-Sanz et al ., 2020; Goring et al ., 2022). All three SI systems known to date utilize the highly polymorphic female- and male-specific S-determinants, but act via different rejection mechanisms.…”

Is self‐incompatibility a reproductive barrier for hybridization in a sympatric species?

“…In phylogenetically closely related species, SI can reduce hybridization events because SI has been linked to interspecific pollen rejection (Harder et al, 1993; McCarthy et al, 1995; Tovar‐Méndez et al, 2014). The genetic mechanisms of SI systems have been extensively developed in commercially important species, but little is known about wild species (Silva and Goring, 2001; Takayama and Isogai, 2005; Goring et al, 2022). Additionally, self‐compatible (SC) species have been proposed to lack a mechanism to reject interspecific pollen (Lewis and Crowe, 1959; Roda and Hopkins, 2019).…”

“…Contrasting strategies of sexual reproduction may have a different contribution to overall reproductive isolation. For example, predominantly self‐pollinating populations with weak self‐incompatibility barriers may have a higher probability of interspecific gene flow and thus be prone to hybridization (Li et al, 2019; Goring et al, 2022).…”