An official website of the United States government
Summary Approximately one‐half of all flowering plants express genetically based physiological mechanisms that prevent self‐fertilisation. One such mechanism, termed RNase‐based self‐incompatibility, employs ribonucleases as the pistil component. Although it is widespread, it has only been characterised in a handful of distantly related families, partly due to the difficulties presented by life history traits of many plants, which complicate genetic research. Many species in the cactus family are known to express self‐incompatibility but the underlying mechanisms remain unknown.We demonstrate the utility of a candidate‐based RNA‐seq approach, combined with some unusual features of self‐incompatibility‐causing genes, which we use to uncover the genetic basis of the underlying mechanisms. Specifically, we assembled transcriptomes fromSchlumbergera truncata(crab cactus or false Christmas cactus), and interrogated them for tissue‐specific expression of candidate genes, structural characteristics, correlation with expressed phenotype(s), and phylogenetic placement.The results were consistent with operation of the RNase‐based self‐incompatibility mechanism in Cactaceae.The finding yields additional evidence that the ancestor of nearly all eudicots possessed RNase‐based self‐incompatibility, as well as a clear path to better conservation practices for one of the most charismatic plant families.
more »
« less
Non‐self recognition‐based self‐incompatibility can alternatively promote or prevent introgression
Summary Self‐incompatibility alleles (S‐alleles), which prevent self‐fertilisation in plants, have historically been expected to benefit from negative frequency‐dependent selection and invade when introduced to a new population through gene flow. However, the most taxonomically widespread form of self‐incompatibility, the ribonuclease‐based system ancestral to the core eudicots, functions through collaborative non‐self recognition, which can affect both short‐term patterns of gene flow and the long‐term process of S‐allele diversification.We analysed a model of S‐allele evolution in two populations connected by migration, focussing on comparisons among the fates of S‐alleles initially unique to each population and those shared among populations.We found that both shared and unique S‐alleles from the population with more unique S‐alleles were usually fitter compared with S‐alleles from the population with fewer S‐alleles. Resident S‐alleles often became extinct and were replaced by migrant S‐alleles, although this outcome could be averted by pollen limitation or biased migration.Collaborative non‐self recognition will usually either result in the whole‐sale replacement of S‐alleles from one population with those from another or else disfavour introgression of S‐alleles altogether.
more »
« less
- Award ID(s):
- 1754246
- PAR ID:
- 10385553
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 231
- Issue:
- 4
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- p. 1630-1643
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract In Mediterranean climates, the timing of seasonal rains determines germination, flowering phenology and fitness. As climate change alters seasonal precipitation patterns, it is important to ask how these changes will affect the phenology and fitness of plant populations. We addressed this question experimentally with the annual plant speciesArabidopsis thaliana.In a first experiment, we manipulated the date of rainfall onset and recorded germination phenology on sand and soil substrates. In a second experiment, we manipulated germination date, growing season length and mid‐season drought to measure their effects on flowering time and fitness. Within each experiment, we manipulated seed dormancy and flowering time using multilocus near‐isogenic lines segregating strong and weak alleles of the seed dormancy geneDOG1and the flowering time geneFRI. We synthesized germination phenology data from the first experiment with fitness functions from the second experiment to project population fitness under different seasonal rainfall scenarios.Germination phenology tracked rainfall onset but was slower and more variable on sand than on soil. Many seeds dispersed on sand in spring and summer delayed germination until the cooler temperatures of autumn. The high‐dormancyDOG1allele also prevented immediate germination in spring and summer. Germination timing strongly affected plant fitness. Fecundity was highest in the October germination cohort and declined in spring germinants. The late floweringFRIallele had lower fecundity, especially in early fall and spring cohorts. Projections of population fitness revealed that: (1) Later onset of autumn rains will negatively affect population fitness. (2) Slow, variable germination on sand buffers populations against fitness impacts of variable spring and summer rainfall. (3) Seasonal selection favours high dormancy and early flowering genotypes in a Mediterranean climate with hot dry summers. The high‐dormancyDOG1allele delayed germination of spring‐dispersed fresh seeds until more favourable early fall conditions, resulting in higher projected population fitness.These findings suggest that Mediterranean annual plant populations are vulnerable to changes in seasonal precipitation, especially in California where rainfall onset is already occurring later. The fitness advantage of highly dormant, early flowering genotypes helps explain the prevalence of this strategy in Mediterranean populations. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
Summary The timing of insects’ daily (feeding, movement) and seasonal (diapause, migration) rhythms affects their population dynamics and distribution. Yet, despite their implications for insect conservation and pest management, the genetic mechanisms underlying variation in timing are poorly understood. Prior research in the European corn borer moth (Ostrinia nubilalis) associated ecotype differences in seasonal diapause and daily activity with genetic variation at the circadian clock geneperiod(per). Here, we demonstrate that populations with divergent allele frequencies atperexhibit differences in daily behavior, seasonal development, and the expression of circadian clock genes. Specifically, later daily activity and shortened diapause were associated with a reduction and delay in the abundance of cyclingpermRNA. CRISPR/Cas9-mediated mutagenesis revealed thatperand/or an intact circadian clock network were essential for the appropriate timing of daily behavior and seasonal responsiveness. Furthermore, a reduction ofpergene dosage inperheterozygous mutants (per-/+) pleiotropically decreased the diapause incidence, shortened post-diapause development, and delayed the timing of daily behavior, in a manner phenotypically reminiscent of wild-type individuals. Altogether, this combination of observational and experimental research strongly suggests thatperis a master regulator of biological rhythms and may contribute to the observed life cycle differences between bivoltine (two generation) and univoltine (one generation)O. nubilalis. HighlightsNatural ecotypes with divergentperiod(per) genotypes differ in their daily and seasonal responses to photoperiodLater daily activity, reduced diapause incidence, and shorter post-diapause development is associated with reducedpermRNA abundanceperis essential for short-day recognition and daily timingReducedpergene dosage shortened post-diapause development and delayed locomotor activitymore » « less
-
Abstract Flowering phenology can vary considerably even at fine spatial scales, potentially leading to temporal reproductive isolation among habitat patches. Climate change could alter flowering synchrony, and hence temporal isolation, if plants in different microhabitats vary in their phenological response to climate change. Despite the importance of temporal isolation in determining patterns of gene flow, and hence population genetic structure and local adaptation, little is known about how changes in climate affect temporal isolation within populations.Here, we use flowering phenology and floral abundance data of 50 subalpine plant species over 44 years to test whether temporal isolation between habitat patches is affected by spring temperature. For each species and year, we analysed temporal separation in peak flowering and flowering overlap between habitat patches separated by 5–950 m.Across our study species, warmer springs were associated with more temporal differentiation in flowering peaks among habitat patches, and less flowering overlap, increasing potential for temporal isolation within populations.Synthesis. By reducing opportunities for mating among plants in nearby habitat patches, our results suggest that warmer springs may reduce opportunities for gene flow within populations, and, consequently, the capacity of plant populations to adapt to environmental changes.more » « less
-
Abstract Effective population size affects the efficacy of selection, rate of evolution by drift and neutral diversity levels. When species are subdivided into multiple populations connected by gene flow, evolutionary processes can depend on global or local effective population sizes. Theory predicts that high levels of diversity might be maintained by gene flow, even very low levels of gene flow, consistent with species long‐term effective population size, but tests of this idea are mostly lacking. Here, we show thatLycaeidesbutterfly populations maintain low contemporary (variance) effective population sizes (e.g. ~200 individuals) and thus evolve rapidly by genetic drift. However, populations harboured high levels of genetic diversity consistent with an effective population size several orders of magnitude larger. We hypothesized that the differences in the magnitude and variability of contemporary versus long‐term effective population sizes were caused by gene flow of sufficient magnitude to maintain diversity but only subtly affect evolution on generational timescales. Consistent with this hypothesis, we detected low but nontrivial gene flow among populations. Furthermore, using short‐term population‐genomic time‐series data, we documented patterns consistent with predictions from this hypothesis, including a weak but detectable excess of evolutionary change in the direction of the mean (migrant gene pool) allele frequencies across populations and consistency in the direction of allele frequency change over time. The documented decoupling of diversity levels and short‐term change by drift inLycaeideshas implications for our understanding of contemporary evolution and the maintenance of genetic variation in the wild.more » « less
