Intraspecific breakdown of self-incompatibility inPhysalis acutifolia(Solanaceae)

Abstract

Variation in mating systems is prevalent throughout angiosperms, with many transitions between outcrossing and selfing above and below the species level. This study documents a new case of an intraspecific breakdown of self-incompatibility in a wild relative of tomatillo, Physalis acutifolia. We used controlled greenhouse crosses to identify self-incompatible (SI) and self-compatible (SC) individuals grown from seed sampled across seven sites across Arizona and New Mexico. We measured fourteen flower and fruit traits to test for trait variation associated with mating system. We also quantified pollen tube growth in vivo and tested for the presence of the S-RNase proteins in SI and SC styles. We found that seed from six of the seven sites produced SI individuals that terminated self pollen tubes in the style and showed detectable S-RNase expression. By contrast, seed from one Arizona site produced SC individuals with no S-RNase expression. These SC individuals displayed typical selfing syndrome traits such as smaller corollas, reduced sigma-anther distances, and a smaller pollen-ovule ratio. We also found plasticity in self-incompatibility as most of the SI individuals became SC and lost S-RNase expression roughly after six months in the greenhouse. While fixed differences in mating systems are known among the self-incompatible wild species and the often self-compatible domesticated tomatillos, our study is the first to demonstrate intraspecific variation in natural populations as well as variation in SI over an individual’s lifespan.

How does a self‐incompatible individual transition to self‐compatibility during its lifetime?

“…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.…”

“…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.…”

“…For plasticity, we divided this summary of the literature into the two major types of conditions (abiotic, biotic). The numbers below each ellipse correspond to studies cited here: (1)Prabha et al, 1982; (2)Lao et al, 2014; (3) Yang et al, 2018; (4) Yamamoto et al, 2019; (5) Travers et al, 2004; (6) Liao et al, 2016; (7) Stephenson et al, 2000; (8) Goodwillie et al, 2004; (9) Pretz and Smith, 2022. Of these, only the study byGoodwillie et al (2004) involved natural populations.…”

Evolutionary and structural aspects of Solanaceae RNases T2

“…On the other hand, Class III is composed of S-RNases, extracellular glycoproteins present in at least three plant families. Their RNase activity is related to the self-incompatibility (SI) system ( Lee et al, 1994 ; Matton et al, 1994 ; Murfett et al, 1994 ; Hua et al, 2008 ; Pretz and Smith, 2022 ), a reproductive barrier that rejects genetically related pollens and accepts unrelated ones ( Kubo et al, 2015 ; Ramanauskas and Igić, 2017 ). In most species displaying self-incompatibility, the discrimination between self- and non-self pollen is controlled by a multi-allelic S -locus ( Torres-Rodríguez et al, 2020 ).…”