Summary
Genetic mutations provide the heritable material for plant adaptation to their environments. At the same time, the environment can affect the mutation rate across plant genomes. However, the ...extent to which environmental plasticity in mutation rates can facilitate or hinder adaptation remains a longstanding and unresolved question. Emerging discoveries of mechanisms affecting mutation rate variability provide opportunities to consider this question in a new light. Links between chromatin states, transposable elements, and DNA repair suggest cases of adaptive mutation rate plasticity could occur. Yet, numerous evolutionary and biological forces are expected to limit the impact of any such mutation rate plasticity on adaptive evolution. Persistent uncertainty about the significance of mutation rate plasticity on adaptation motivates new experimental and theoretical research relevant to understanding plant responses in changing environments.
Since the first half of the twentieth century, evolutionary theory has been dominated by the idea that mutations occur randomly with respect to their consequences
. Here we test this assumption with ...large surveys of de novo mutations in the plant Arabidopsis thaliana. In contrast to expectations, we find that mutations occur less often in functionally constrained regions of the genome-mutation frequency is reduced by half inside gene bodies and by two-thirds in essential genes. With independent genomic mutation datasets, including from the largest Arabidopsis mutation accumulation experiment conducted to date, we demonstrate that epigenomic and physical features explain over 90% of variance in the genome-wide pattern of mutation bias surrounding genes. Observed mutation frequencies around genes in turn accurately predict patterns of genetic polymorphisms in natural Arabidopsis accessions (r = 0.96). That mutation bias is the primary force behind patterns of sequence evolution around genes in natural accessions is supported by analyses of allele frequencies. Finally, we find that genes subject to stronger purifying selection have a lower mutation rate. We conclude that epigenome-associated mutation bias
reduces the occurrence of deleterious mutations in Arabidopsis, challenging the prevailing paradigm that mutation is a directionless force in evolution.
Understanding the controls on the amount and persistence of soil organic carbon (C) is essential for predicting its sensitivity to global change. The response may depend on whether C is unprotected, ...isolated within aggregates, or protected from decomposition by mineral associations. Here, we present a global synthesis of the relative influence of environmental factors on soil organic C partitioning among pools, abundance in each pool (mg C g−1 soil), and persistence (as approximated by radiocarbon abundance) in relatively unprotected particulate and protected mineral‐bound pools. We show that C within particulate and mineral‐associated pools consistently differed from one another in degree of persistence and relationship to environmental factors. Soil depth was the best predictor of C abundance and persistence, though it accounted for more variance in persistence. Persistence of all C pools decreased with increasing mean annual temperature (MAT) throughout the soil profile, whereas persistence increased with increasing wetness index (MAP/PET) in subsurface soils (30–176 cm). The relationship of C abundance (mg C g−1 soil) to climate varied among pools and with depth. Mineral‐associated C in surface soils (<30 cm) increased more strongly with increasing wetness index than the free particulate C, but both pools showed attenuated responses to the wetness index at depth. Overall, these relationships suggest a strong influence of climate on soil C properties, and a potential loss of soil C from protected pools in areas with decreasing wetness. Relative persistence and abundance of C pools varied significantly among land cover types and soil parent material lithologies. This variability in each pool's relationship to environmental factors suggests that not all soil organic C is equally vulnerable to global change. Therefore, projections of future soil organic C based on patterns and responses of bulk soil organic C may be misleading.
In the first global meta‐analysis to examine both radiocarbon and C concentrations among different soil C pools, we found that three critical carbon pools (free particulate, occluded particulate, and mineral associated) respond differently to climate. Moisture had an almost equal influence as temperature on C persistence and abundance, highlighting the need for climate change studies focused on moisture manipulations. The strong variation in pool characteristics and their relationship to environmental factors indicates that we need to go beyond bulk soil carbon measurements to understand and model the responses of soil organic carbon to global change; it is critical to evaluate distinct pools as response variables.
Mutation is the source of all heritable diversity, the essential material of evolution and breeding. While mutation rates are often regarded as constant, variability in mutation rates has been ...observed at nearly every level-varying across mutation types, genome locations, gene functions, epigenomic contexts, environmental conditions, genotypes, and species. This mutation rate variation arises from differential rates of DNA damage, repair, and transposable element activation and insertion that together produce what is measured by DNA mutation rates. We review historical and recent investigations into the causes and consequences of mutation rate variability in plants by focusing on the mechanisms shaping this variation. Emerging mechanistic models point to the evolvability of mutation rate variation across genomes via mechanisms that target DNA repair, shaping the diversification of plants at phenotypic and genomic scales.
Genome analyses reveal that several plants have lost a major part of the immune system.
Abstract
Plant innate immunity relies on nucleotide binding leucine-rich repeat receptors (NLRs) that recognize ...pathogen-derived molecules and activate downstream signaling pathways. We analyzed the variation in NLR gene copy number and identified plants with a low number of NLR genes relative to sister species. We specifically focused on four plants from two distinct lineages, one monocot lineage (Alismatales) and one eudicot lineage (Lentibulariaceae). In these lineages, the loss of NLR genes coincides with loss of the well-known downstream immune signaling complex ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)/PHYTOALEXIN DEFICIENT 4 (PAD4). We expanded our analysis across whole proteomes and found that other characterized immune genes were absent only in Lentibulariaceae and Alismatales. Additionally, we identified genes of unknown function that were convergently lost together with EDS1/PAD4 in five plant species. Gene expression analyses in Arabidopsis (Arabidopsis thaliana) and Oryza sativa revealed that several homologs of the candidates are differentially expressed during pathogen infection, drought, and abscisic acid treatment. Our analysis provides evolutionary evidence for the rewiring of plant immunity in some plant lineages, as well as the coevolution of the EDS1/PAD4 pathway and drought responses.
Interdisciplinary syntheses are needed to scale up discovery of the environmental drivers and molecular basis of adaptation in nature. Here we integrated novel approaches using whole genome ...sequences, satellite remote sensing, and transgenic experiments to study natural loss-of-function alleles associated with drought histories in wild
. The genes we identified exhibit population genetic signatures of parallel molecular evolution, selection for loss-of-function, and shared associations with flowering time phenotypes in directions consistent with longstanding adaptive hypotheses seven times more often than expected by chance. We then confirmed predicted phenotypes experimentally in transgenic knockout lines. These findings reveal the importance of drought timing to explain the evolution of alternative drought tolerance strategies and further challenge popular assumptions about the adaptive value of genetic loss-of-function in nature. These results also motivate improved species-wide sequencing efforts to better identify loss-of-function variants and inspire new opportunities for engineering climate resilience in crops.
Rates of sequence evolution in plastid genomes are generally low, but numerous angiosperm lineages exhibit accelerated evolutionary rates in similar subsets of plastid genes. These genes include ...clpP1 and accD, which encode components of the caseinolytic protease (CLP) and acetyl-coA carboxylase (ACCase) complexes, respectively. Whether these extreme and repeated accelerations in rates of plastid genome evolution result from adaptive change in proteins (i.e., positive selection) or simply a loss of functional constraint (i.e., relaxed purifying selection) is a source of ongoing controversy. To address this, we have taken advantage of the multiple independent accelerations that have occurred within the genus Silene (Caryophyllaceae) by examining phylogenetic and population genetic variation in the nuclear genes that encode subunits of the CLP and ACCase complexes. We found that, in species with accelerated plastid genome evolution, the nuclear-encoded subunits in the CLP and ACCase complexes are also evolving rapidly, especially those involved in direct physical interactions with plastid-encoded proteins. A massive excess of nonsynonymous substitutions between species relative to levels of intraspecific polymorphism indicated a history of strong positive selection (particularly in CLP genes). Interestingly, however, some species are likely undergoing loss of the native (heteromeric) plastid ACCase and putative functional replacement by a duplicated cytosolic (homomeric) ACCase. Overall, the patterns of molecular evolution in these plastid-nuclear complexes are unusual for anciently conserved enzymes. They instead resemble cases of antagonistic coevolution between pathogens and host immune genes. We discuss a possible role of plastid-nuclear conflict as a novel cause of accelerated evolution.
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