Regional genetic diversity in circadian period in Boechera stricta populations is high relative to the global range of diversity in Arabidopsis

Circadian clocks manifest adaptations to predictable 24-h fluctuations in the exogenous environment, but it has yet to be determined why the endogenous circadian period length in the wild varies genetically around the hypothesized optimum of 24 h. We quantified genetic variation in circadian period in leaf movement in 30 natural populations of the Arabidopsis relative Boechera stricta sampled within only 1° of latitude but across an elevational gradient spanning 2460−3300 m in the Rocky Mountains. Measuring over 3800 plants from 473 maternal families (7−20 per population), we found genetic variation that was of similar magnitude among vs. within populations, with population means varying between 21.9−24.9 h and maternal family means within populations varying by up to ~6 h. After statistically factoring out spatial autocorrelation at the habitat extremes, we found that elevation explained a significant proportion of genetic variation in circadian period such that higher-elevation populations had shorter mean period lengths and less within-population variation. Environmental data indicate that these spatial trends could be related to steep regional climatic gradients in temperature, precipitation, and their intra-annual variability. Our findings provide evidence that spatially fine-grained environmental heterogeneity contributes to naturally occurring genetic diversity in circadian traits in wild populations.

Rhizosphere microbes influence host circadian clock function

The circadian clock is an important determinant of fitness that is entrained by local conditions. Aside from abiotic factors, individual pathogenic soil bacteria affect circadian clock function in plant hosts. Yet, in nature, plants interact with diverse microbial communities, and the effect of complex communities on clock function remains unclear. In Arabidopsis thaliana and its wild relative, Boechera stricta, we used diverse rhizosphere inoculates and host genotypes to test the effect of complex rhizosphere microbial communities on the host circadian clock. Arabidopsis thaliana plants with an intact rhizosphere microbiome expressed a circadian period closer to 24h in duration and significantly shorter (by 48 minutes on average) relative to plants grown with a disrupted microbiome. Wild-type host genotypes of A. thaliana differed in clock sensitivity to microbes, with one genotype (Landsberg erecta) expressing a 119-minute difference in circadian period length across rhizosphere microbial treatments. A similar pattern of clock sensitivity to soil microbes was observed in B. stricta. Finally, rhizosphere microbes collected from the mutant genotype toc1-21 of A. thaliana with a short-period phenotype and used as inoculate significantly shortened the long-period phenotype of the clock mutant genotype ztl-1. The results indicate that complex rhizosphere microbial communities affect host clock function.

The ecological, genetic and genomic architecture of local adaptation and population differentiation in Boechera stricta

Differential local adaptation restricts gene flow between populations inhabiting distinct environments, resulting in isolation by adaptation. In addition to the statistical inferences of genotype–environment associations, an integrative approach is needed to investigate the effect of local adaptation on population divergence at the ecological, genetic and genomic scale. Here, we combine reciprocal transplant, genome–environment association and QTL mapping to investigate local adaptation in Boechera stricta (Drummond's rockcress). With reciprocal transplant experiment, we found local genetic groups exhibit phenotypic characteristics corresponding to the distinct selection forces from different water availability. At the genetic level, the local allele of a major fitness QTL confers higher and sturdier flowering stalks, maximizing the fecundity fitness component under sufficient water supply, and its genetic variation is associated with precipitation across the landscape. At the genomewide scale, we further showed that multiple loci associated with precipitation are highly differentiated between genetic groups, suggesting that local adaptation has a widespread effect on reducing gene flow. This study provides one of the few comprehensive examples demonstrating how local adaptation facilitates population divergence at the trait, gene and genome level.

Costs of reproduction under experimental climate change across elevations in the perennial forb Boechera stricta

Investment in current reproduction can reduce future fitness by depleting resources needed for maintenance, particularly under environmental stress. These trade-offs influence life-history evolution. We tested whether climate change alters the future-fitness costs of current reproduction in a large-scale field experiment of Boechera stricta (Brassicaceae). Over 6 years, we simulated climate change along an elevational gradient in the Rocky Mountains through snow removal, which accelerates snowmelt and reduces soil water availability. Costs of reproduction were greatest in arid, lower elevations, where high initial reproductive effort depressed future fitness. At mid-elevations, initial reproduction augmented subsequent fitness in benign conditions, but pronounced costs emerged under snow removal. At high elevation, snow removal dampened costs of reproduction by prolonging the growing season. In most scenarios, failed reproduction in response to resource limitation depressed lifetime fecundity. Indeed, fruit abortion only benefited high-fitness individuals under benign conditions. We propose that climate change could shift life-history trade-offs in an environment-dependent fashion, possibly favouring early reproduction and short lifespans in stressful conditions.

Whether Gametophytes Are Reduced or Unreduced in Angiosperms Might Be Determined Metabolically

In angiosperms, meiotic failure coupled with the formation of genetically unreduced gametophytes in ovules (apomeiosis) constitute major components of gametophytic apomixis. These aberrant developmental events are generally thought to be caused by mutation. However, efforts to locate the responsible mutations have failed. Herein, we tested a fundamentally different hypothesis: apomeiosis is a polyphenism of meiosis, with meiosis and apomeiosis being maintained by different states of metabolic homeostasis. Microarray analyses of ovules and pistils were used to differentiate meiotic from apomeiotic processes in Boechera (Brassicaceae). Genes associated with translation, cell division, epigenetic silencing, flowering, and meiosis characterized sexual Boechera (meiotic). In contrast, genes associated with stress responses, abscisic acid signaling, reactive oxygen species production, and stress attenuation mechanisms characterized apomictic Boechera (apomeiotic). We next tested whether these metabolic differences regulate reproductive mode. Apomeiosis switched to meiosis when premeiotic ovules of apomicts were cultured on media that increased oxidative stress. These treatments included drought, starvation, and H2O2 applications. In contrast, meiosis switched to apomeiosis when premeiotic pistils of sexual plants were cultured on media that relieved oxidative stress. These treatments included antioxidants, glucose, abscisic acid, fluridone, and 5-azacytidine. High-frequency apomeiosis was initiated in all sexual species tested: Brassicaceae, Boechera stricta, Boechera exilis, and Arabidopsis thaliana; Fabaceae, Vigna unguiculata; Asteraceae, Antennaria dioica. Unreduced gametophytes formed from ameiotic female and male sporocytes, first division restitution dyads, and nucellar cells. These results are consistent with modes of reproduction and types of apomixis, in natural apomicts, being regulated metabolically.

The evolution of sex is tempered by costly hybridization in Boechera (rock cress)

Even after decades of research, the evolution of sex remains an enigma in evolutionary biology. Typically, research addresses the costs of sex and asexuality to characterize the circumstances in which one reproductive system is more favorable. Yet surprisingly few studies address the influence of common traits that are obligately correlated with asexuality, including hybridization and polyploidy; even though these traits have substantial impacts on selective patterns. In particular, hybridization is well-known to alter trait expression; these alterations may themselves represent a cost of sex. We examined the role of reproductive isolation in the formation of de novo hybrid lineages between two widespread species in the ecological model system Boechera. Of 664 crosses between Boechera stricta and Boechera retrofracta, 17% of crosses produced F1 fruits. This suggests that postmating prezygotic barriers, i.e. pollen-pistil interactions, form the major barrier to hybrid success in this system. These interactions are asymmetrical, with 110 F1 fruits produced when B. stricta was the maternal parent. This asymmetry was confirmed using a chloroplast phylogeny of wild-collected B. stricta, B. retrofracta, and hybrids, which showed that most hybrids have a B. stricta chloroplast haplotype. We next compared fitness of F2 hybrids and selfed parental B. stricta lines, finding that F2 fitness was reduced by substantial hybrid sterility. Our results suggest that multiple reproductively isolating barriers likely influence the formation and fitness of hybrid lineages in the wild, and that these costs of hybridization likely have profound impacts on the costs of sex in the natural environment.

Genome draft of the Arabidopsis relative Pachycladon cheesemanii reveals novel strategies to tolerate New Zealand’s high ultraviolet B radiation environment

Background Pachycladon cheesemanii is a close relative of Arabidopsis thaliana and is an allotetraploid perennial herb which is widespread in the South Island of New Zealand. It grows at altitudes of up to 1000 m where it is subject to relatively high levels of ultraviolet (UV)-B radiation. To gain first insights into how Pachycladon copes with UV-B stress, we sequenced its genome and compared the UV-B tolerance of two Pachycladon accessions with those of two A. thaliana accessions from different altitudes. Results A high-quality draft genome of P. cheesemanii was assembled with a high percentage of conserved single-copy plant orthologs. Synteny analysis with genomes from other species of the Brassicaceae family found a close phylogenetic relationship of P. cheesemanii with Boechera stricta from Brassicaceae lineage I. While UV-B radiation caused a greater growth reduction in the A. thaliana accessions than in the P. cheesemanii accessions, growth was not reduced in one P. cheesemanii accession. The homologues of A. thaliana UV-B radiation response genes were duplicated in P. cheesemanii, and an expression analysis of those genes indicated that the tolerance mechanism in P. cheesemanii appears to differ from that in A. thaliana. Conclusion Although the P. cheesemanii genome shows close similarity with that of A. thaliana, it appears to have evolved novel strategies allowing the plant to tolerate relatively high UV-B radiation.