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1. Phenological and fitness responses to climate warming depend upon genotype and competitive neighbourhood in Arabidopsis thaliana

   https://doi.org/10.1111/1365-2435.13262  

   Taylor, Mark A. ; Cooper, Martha D. ; Schmitt, Johanna ; Manzaneda, ed., Antonio J. ( January 2019 , Functional Ecology)

   Increasing temperatures during climate change are known to alter the phenology across diverse plant taxa, but the evolutionary outcomes of these shifts are poorly understood. Moreover, plant temperature‐sensing pathways are known to interact with competition‐sensing pathways, yet there remains little experimental evidence for how genotypes varying in temperature responsiveness react to warming in realistic competitive settings.

   We compared flowering time and fitness responses to warming and competition for two near‐isogenic lines (NILs) ofArabidopsis thalianatransgressively segregating temperature‐sensitive and temperature‐insensitive alleles for major‐effect flowering time genes. We grew focal plants of each genotype in intraspecific and interspecific competition in four treatments contrasting daily temperature profiles in summer and fall under contemporary and warmed conditions. We measured phenology and fitness of focal plants to quantify plastic responses to season, temperature and competition and the dependence of these responses on flowering time genotype.

   The temperature‐insensitive NIL was constitutively early flowering and less fit, except in a future‐summer climate in which its fitness was higher than the later flowering, temperature‐sensitive NIL in low competition. The late‐flowering NIL showed accelerated flowering in response to intragenotypic competition and to increased temperature in the summer but delayed flowering in the fall. However, its fitness fell with rising temperatures in both seasons, and in the fall its marginal fitness gain from decreasing competition was diminished in the future.

   Functional alleles at temperature‐responsive genes were necessary for plastic responses to season, warming and competition. However, the plastic genotype was not the most fit in every experimental condition, becoming less fit than the temperature‐canalized genotype in the warm summer treatment.

   Climate change is often predicted to have deleterious effects on plant populations, and our results show how increased temperatures can act through genotype‐dependent phenology to decrease fitness. Furthermore, plasticity is not necessarily adaptive in rapidly changing environments since a nonplastic genotype proved fitter than a plastic genotype in a warming climate treatment.

   Aplain language summaryis available for this article.

    

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2. Population structure, landscape genomics, and genetic signatures of adaptation to exotic disease pressure in Cornus florida L.—Insights from GWAS and GBS data

   https://doi.org/10.1111/jse.12592  

   Pais, Andrew L. ; Whetten, Ross W. ; Xiang, Qiu‐Yun ( May 2020 , Journal of Systematics and Evolution)

   Understanding the consequences of exotic diseases on native forests is important to evolutionary ecology and conservation biology because exotic pathogens have drastically altered US eastern deciduous forests.Cornus floridaL. (flowering dogwood tree) is one such species facing heavy mortality. Characterizing the genetic structure ofC. floridapopulations and identifying the genetic signature of adaptation to dogwood anthracnose (an exotic pathogen responsible for high mortality) remain vital for conservation efforts. By integrating genetic data from genotype by sequencing (GBS) of 289 trees across the host species range and distribution of disease, we evaluated the spatial patterns of genetic variation and population genetic structure ofC. floridaand compared the pattern to the distribution of dogwood anthracnose. Using genome‐wide association study and gradient forest analysis, we identified genetic loci under selection and associated with ecological and diseased regions. The results revealed signals of weak genetic differentiation of three or more subgroups nested within two clusters—explaining up to 2%–6% of genetic variation. The groups largely corresponded to the regions within and outside the eastern Hot‐Continental ecoregion, which also overlapped with areas within and outside the main distribution of dogwood anthracnose. The fungal sequences contained in the GBS data of sampled trees bolstered visual records of disease at sampled locations and were congruent with the reported range ofDiscula destructiva, suggesting that fungal sequences within‐host genomic data were informative for detecting or predicting disease. The genetic diversity between populations at diseased vs. disease‐free sites across the range ofC. floridashowed no significant difference. We identified 72 single‐nucleotide polymorphisms (SNPs) from 68 loci putatively under selection, some of which exhibited abrupt turnover in allele frequencies along the borders of the Hot‐Continental ecoregion and the range of dogwood anthracnose. One such candidate SNP was independently identified in two prior studies as a possible L‐type lectin‐domain containing receptor kinase. Although diseased and disease‐free areas do not significantly differ in genetic diversity, overall there are slight trends to indicate marginally smaller amounts of genetic diversity in disease‐affected areas. Our results were congruent with previous studies that were based on a limited number of genetic markers in revealing high genetic variation and weak population structure inC. florida.

    

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3. Natural variations of growth thermo‐responsiveness determined by SAUR 26/27/28 proteins in Arabidopsis thaliana

   https://doi.org/10.1111/nph.15956  

   Wang, Zhixue ; Yang, Leiyun ; Liu, Zhenhua ; Lu, Minghui ; Wang, Minghui ; Sun, Qi ; Lan, Yiheng ; Shi, Tieliu ; Wu, Dianxing ; Hua, Jian ( June 2019 , New Phytologist)

   How diversity in growth thermo‐responsiveness is generated for local adaptation is a long‐standing biological question. We investigated molecular genetic basis of natural variations in thermo‐responsiveness of plant architecture inArabidopsis thaliana.

   We measured the extent of rosette architecture at 22°C and 28°C in a set of 69 natural accessions and determined their thermo‐responsiveness of plant architecture. A genome‐wide association study was performed to identify major loci for variations in thermo‐responsiveness.

   TheSAUR26subfamily, a new subfamily ofSAURgenes, was identified as a major locus for the thermo‐responsive architecture variations. The expression ofSAUR26/27/28is modulated by temperature andPIF4. Extensive natural polymorphisms in these genes affect theirRNAexpression levels and protein activities and influence the thermo‐responsiveness of plant architecture. In addition, theSAUR26subfamily genes exhibit a high variation frequency and their variations are associated with the local temperature climate.

   This study reveals that theSAUR26subfamily is a key variation for thermo‐responsive architecture and suggests a preference for generating diversity for local adaptation through signaling connectors.

    

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4. Precipitation timing and soil substrate drive phenology and fitness of Arabidopsis thaliana in a Mediterranean environment

   https://doi.org/10.1111/1365-2435.14391  

   Martínez‐Berdeja, Alejandra ; Okada, Miki ; Cooper, Martha D. ; Runcie, Daniel E. ; Burghardt, Liana T. ; Schmitt, Johanna ( July 2023 , Functional Ecology)

   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.

    

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5. Adaptive and nonadaptive causes of heterogeneity in genetic differentiation across the Mimulus guttatus genome

   https://doi.org/10.1111/mec.16087  

   Colicchio, Jack M. ; Hamm, Lauren N. ; Verdonk, Hannah E. ; Kooyers, Nicholas J. ; Blackman, Benjamin K. ( August 2021 , Molecular Ecology)

   Genetic diversity becomes structured among populations over time due to genetic drift and divergent selection. Although population structure is often treated as a uniform underlying factor, recent resequencing studies of wild populations have demonstrated that diversity in many regions of the genome may be structured quite dissimilar to the genome‐wide pattern. Here, we explored the adaptive and nonadaptive causes of such genomic heterogeneity using population‐level, whole genome resequencing data obtained from annualMimulus guttatusindividuals collected across a rugged environment landscape. We found substantial variation in how genetic differentiation is structured both within and between chromosomes, although, in contrast to other studies, known inversion polymorphisms appear to serve only minor roles in this heterogeneity. In addition, much of the genome can be clustered into eight among‐population genetic differentiation patterns, but only two of these clusters are particularly consistent with patterns of isolation by distance. By performing genotype‐environment association analysis, we also identified genomic intervals where local adaptation to specific climate factors has accentuated genetic differentiation among populations, and candidate genes in these windows indicate climate adaptation may proceed through changes affecting specialized metabolism, drought resistance, and development. Finally, by integrating our findings with previous studies, we show that multiple aspects of plant reproductive biology may be common targets of balancing selection and that variants historically involved in climate adaptation among populations have probably also fuelled rapid adaptation to microgeographic environmental variation within sites.

    

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