How does a self‐incompatible individual transition to self‐compatibility during its lifetime?
Year: 2023
Type: article
Abstract: The transition from self-incompatibility (SI) to self-compatibility (SC) has been argued to be one of the most common and influential evolutionary changes in flowering plants (Igic et al., 2008). While the loss of SI may result in an evolutionary dead-end (e.g., due to inbreeding depression; Wright et al., 2013), the ability to accept self-pollen may also be advantageous, providing reproductive assurance when species expand to new areas (e.g., Broz et al., 2017) or caused by pollinator limitation (Fenster and Ritland, 1994). These benefits experienced by individuals with stable, genetically based self-compatibility may also benefit individuals that can change their mating system over their lifespan (Stephenson et al., 2000; Goodwillie et al., 2005). Nevertheless, compared to fixed differences in compatibility between individuals, populations, or species, we know relatively little about the loss of SI within an individual's lifespan, from how it happens developmentally to its frequency and significance in nature. At the scale of an individual lifetime, we can divide the transition from SI to SC into two categories, phenotypic plasticity and developmental decay. Phenotypic plasticity occurs when a genotype can produce multiple different phenotypes depending on external stimuli (Pigliucci et al., 2006). For example, an initially SI individual may transition to SC due to an environmental stressor and revert to SI when the stressor is removed (Figure 1A). Alternatively, plants may exhibit progressive developmental decay of SI that transitions irreversibly to SC (Figure 1B). While this pattern of loss of SI with age has often been referred to as plasticity (e.g., Mena-Ali and Stephenson, 2007; Liao et al., 2016), we favor the term developmental decay because this process does not depend on an external stimulus and is a predictable outcome of ontogeny. For both plastic changes in compatibility and developmental decay, the loss of SI could occur at the level of an entire plant, an inflorescence, or a single flower, although we do not have evidence of the phenomenon for all of these possibilities (Figure 2). Most evidence for plasticity in compatibility comes from manipulative experiments in the greenhouse or growth chambers. For example, artificial pollination studies in Solanum carolinense showed that plants that receive only self-pollen for the first 20 flowers are subsequently more likely to accept self-pollen and produce fruit (Travers et al., 2004). Abiotic factors can also influence compatibility. For instance, in Ipomoea fistulosa, heat can induce the SC phenotype, but flowers will revert to SI after a day of normal temperatures (Prabha et al., 1982). Similarly, artificial exposure to elevated temperature, CO2, or salt can induce SC in Brassicaceae (Lao et al., 2014; Yang et al., 2018; Yamamoto et al., 2019), a lineage with sporophytic self-incompatibility (SSI). The calcium signaling involved in SSI systems may be particularly susceptible to these abiotic perturbations, suggesting these might be the focal taxa to test for plastic expression of SC under stressful conditions in nature. Developmental decay of SI has been studied in several species but is best documented in association with flower age. For instance, in Leptosiphon jepsonii, self-pollen tube growth is inhibited in first day flowers, but as the flowers age the self-pollen tubes will research the ovule, resulting in delayed selfing (Goodwillie et al., 2004). This phenotype varies across natural populations, with some individuals having flowers that accept self-pollen immediately upon opening and others showing delayed selfing (Goodwillie and Ness, 2005). There are no examples of the decay of SI within an inflorescence (e.g., early flowers being SI, and later flowers being SC), but they might be anticipated given that other phenotypes, like sex expression, can depend on location within inflorescences (Diggle et al., 1994). There is, however, one documented case in Solanaceae in which a whole plant will transition from SI to SC within a lifespan, with older individuals producing exclusively SC flowers (Pretz and Smith, 2022). The above examples of developmental decay of SI taxa with gametophytic self-incompatibility (GSI) demonstrate that the potential for progressive loss of self-pollen rejection with age transcends the underlying genetic system. To the extent that they have been studied, the mechanisms involved in shifts to self-compatibility during a lifetime, often share similarities with the mechanisms responsible for stable, genetically fixed transitions to SC. For example, in GSI systems, decreases in S-RNase expression are associated with loss of SI through both plasticity (Mena-Ali and Stephenson, 2007) and developmental decay (Pretz and Smith, 2022), much like the loss of S-RNase function or expression found in heritable SI-SC transitions (e.g., Broz et al., 2017). The precise molecular underpinnings, e.g., reduced transcription due to a regulatory protein or targeted degradation of S-RNase transcripts, have not been identified, but any changes in SI during a lifetime would have to involve changes in gene regulation. In SSI systems, the molecular basis for plastic changes have been dissected in greater detail and sometimes involve the S-locus pollen and pistil factors (SCR and SRK) that are often implicated in evolutionary transitions (Mable, 2008). For instance, high temperatures cause the loss of SI by disrupting SRK localization (Yamamoto et al., 2019), but a wide range of physiological mechanisms independent of the S-locus are involved in the loss of SI with exposure to salt (Yang et al., 2018). Overall, given the complexity of SI systems and their modifiers, we predict that further research will reveal a broad array of molecular, physiological, and developmental processes that contribute to plasticity and decay of SI. It is important to note that transitions to SC during an individual's lifespan may have varying fitness consequences. Even plants that become self-fertile may produce fewer seeds from self-pollination than from outcross pollination (Travers et al., 2004). In the case of the decay of SI in older flowers or plants, most offspring may still be the result of outcrossing, for example, if cross pollen outcompetes self-pollen in reaching the ovules. We suspect that developmental decay or plastic transitions to SC are far more common in flowering plants than currently known and that this latent ability may be hiding in systems that are largely outcrossing (Levin, 1996). Discovering additional species possessing the ability to convert to an SC phenotype during a lifetime is only the first step toward understanding the significance of this phenomenon. While it is relatively straightforward to document plasticity or developmental decay in the greenhouse, the occurrence of these processes in natural populations has only been studied in a few species (Stephenson et al., 2000; Goodwillie et al., 2004), leaving a major gap in our understanding of plant reproductive biology. Nevertheless, the same factors that trigger plasticity in SI in artificial experiments occur in nature, and there, the plastic loss of SI may often be adaptive. For instance, abiotic stressors that induce the SC phenotype could allow a plant to reproduce quickly when conditions do not support a long flowering period to wait for the arrival of outcross pollen. Similarly, we expect plants to benefit from reproductive assurance with the developmental decay of SI, such as if a short-lived annual relies on specialized pollinators (Pretz and Smith, 2022). While the frequency of these changes in SI over a lifespan across flowering plants remains far from clear, the flexibility in compatibility demonstrated in only the handful of well-studied systems reinforces the notion that SI and SC do not represent binary states, but instead a spectrum, from the species level down to the finest of temporal scales within a single flower. Do the different mechanisms for within-lifespan changes in SI vary with the type of incompatibility? Specifically, are plastic changes more common with SSI and is developmental decay more common with GSI? How reversible are the plastic changes in SI? And does the timing and extent of the imposed condition influence the potential for reversibility? How often do the molecular mechanisms responsible for plasticity in SI or developmental decay mirror those responsible for fixed differences in compatibility? To what degree are the within-lifespan changes in SI documented in artificial settings also found in nature? For example, do natural populations of species of Brassicaceae show plastic loss of SI under extreme heat? How common is the ability to change compatibility within a lifespan across flowering plants? How often is this capacity adaptive? C.P. and S.D.S. contributed equally to conceptualization, drafting, and writing. C.P. gratefully acknowledges funding from the National Science Foundation Graduate Research Fellowship (DGE 1650115). The authors also thank three anonymous reviewers for constructive feedback on an earlier version of the manuscript.
Source: American Journal of Botany
DOI: 10.1002/ajb2.16150
Authors: Chelsea Pretz, Stacey D. Smith
Institutions: University of Colorado Boulder, University of Colorado System
Language: English
Topic: Plant Reproductive Biology
Subfield: Molecular Biology
Domain: Life Sciences
Open Access status: bronze
Funder: National Science Foundation
OpenAlex ID: W4323074116