Crop adaptation to climate change: An evolutionary perspective.

The disciplines of evolutionary biology and plant and animal breeding have been intertwined throughout their development, with responses to artificial selection yielding insights into the action of natural selection and evolutionary biology providing statistical and conceptual guidance for modern breeding. Here we offer an evolutionary perspective on a grand challenge of the 21st century: feeding humanity in the face of climate change. We first highlight promising strategies currently under way to adapt crops to current and future climate change. These include methods to match crop varieties with current and predicted environments and to optimize breeding goals, management practices, and crop microbiomes to enhance yield and sustainable production. We also describe the promise of crop wild relatives and recent technological innovations such as speed breeding, genomic selection, and genome editing for improving environmental resilience of existing crop varieties or for developing new crops. Next, we discuss how methods and theory from evolutionary biology can enhance these existing strategies and suggest novel approaches. We focus initially on methods for reconstructing the evolutionary history of crops and their pests and symbionts, because such historical information provides an overall framework for crop-improvement efforts. We then describe how evolutionary approaches can be used to detect and mitigate the accumulation of deleterious mutations in crop genomes, identify alleles and mutations that underlie adaptation (and maladaptation) to agricultural environments, mitigate evolutionary trade-offs, and improve critical proteins. Continuing feedback between the evolution and crop biology communities will ensure optimal design of strategies for adapting crops to climate change.

Interspecific Variation in the Unsaturation Level of Seed Oils Were Associated With the Expression Pattern Shifts of Duplicated Desaturase Genes and the Potential Role of Other Regulatory Genes.

Seed oils are of great economic importance both for human consumption and industrial applications. The nutritional quality and industrial value of seed oils are mostly determined by their fatty acid profiles, especially the relative proportions of unsaturated fatty acids. Tree peony seed oils have recently been recognized as novel edible oils enriched in α-linolenic acid (ALA). However, congeneric species, such as Paeonia ostii and P. ludlowii, showed marked variation in the relative proportions of different unsaturated fatty acids. By comparing the dynamics of fatty acid accumulation and the time-course gene expression patterns between P. ostii and P. ludlowii, we identified genes that were differentially expressed between two species in developing seeds, and showed congruent patterns of variation between expression levels and phenotypes. In addition to the well-known desaturase and acyltransferase genes associated with fatty acid desaturation, among them were some genes that were conservatively co-expressed with the desaturation pathway genes across phylogenetically distant ALA-rich species, including Camelina sativa and Perilla frutescens. Go enrichment analysis revealed that these genes were mainly involved in transcriptional regulation, protein post-translational modification and hormone biosynthesis and response, suggesting that the fatty acid synthesis and desaturation pathway might be subject to multiple levels of regulation.

Genetic and phenotypic analyses indicate that resistance to flooding stress is uncoupled from performance in cultivated sunflower.

Given the rising risk of extreme weather caused by climate change, enhancement of abiotic stress resistance in crops is increasingly urgent. But will the development of stress-resistant cultivars come at the cost of yield under ideal conditions? We hypothesize that this need not be inevitable, because resistance alleles with minimal pleiotropic costs may evade artificial selection and be retained in crop germplasm. Genome-wide association (GWA) analyses for variation in plant performance and flooding response were conducted in cultivated sunflower, a globally important oilseed. We observed broad variation in flooding responses among genotypes. Flooding resistance was not strongly correlated with performance in control conditions, suggesting no inherent trade-offs. Consistent with this finding, we identified a subset of loci conferring flooding resistance, but lacking antagonistic effects on growth. Genetic diversity loss at candidate genes underlying these loci was significantly less than for other resistance genes during cultivated sunflower evolution. Despite bottlenecks associated with domestication and improvement, low-cost resistance alleles remain within the cultivated sunflower gene pool. Thus, development of cultivars that are both flooding-tolerant and highly productive should be straightforward. Results further indicate that estimates of pleiotropic costs from GWA analyses explain, in part, patterns of diversity loss in crop genomes.

Sunflower pan-genome analysis shows that hybridization altered gene content and disease resistance.

Domesticated plants and animals often display dramatic responses to selection, but the origins of the genetic diversity underlying these responses remain poorly understood. Despite domestication and improvement bottlenecks, the cultivated sunflower remains highly variable genetically, possibly due to hybridization with wild relatives. To characterize genetic diversity in the sunflower and to quantify contributions from wild relatives, we sequenced 287 cultivated lines, 17 Native American landraces and 189 wild accessions representing 11 compatible wild species. Cultivar sequences failing to map to the sunflower reference were assembled de novo for each genotype to determine the gene repertoire, or 'pan-genome', of the cultivated sunflower. Assembled genes were then compared to the wild species to estimate origins. Results indicate that the cultivated sunflower pan-genome comprises 61,205 genes, of which 27% vary across genotypes. Approximately 10% of the cultivated sunflower pan-genome is derived through introgression from wild sunflower species, and 1.5% of genes originated solely through introgression. Gene ontology functional analyses further indicate that genes associated with biotic resistance are over-represented among introgressed regions, an observation consistent with breeding records. Analyses of allelic variation associated with downy mildew resistance provide an example in which such introgressions have contributed to resistance to a globally challenging disease.

Transient Stability of Epigenetic Population Differentiation in a Clonal Invader.

Epigenetic variation may play an important role in how plants cope with novel environments. While significant epigenetic differences among plants from contrasting habitats have often been observed in the field, the stability of these differences remains little understood. Here, we combined field monitoring with a multi-generation common garden approach to study the dynamics of DNA methylation variation in invasive Chinese populations of the clonal alligator weed (Alternanthera philoxeroides). Using AFLP and MSAP markers, we found little variation in DNA sequence but substantial epigenetic population differentiation. In the field, these differences remained stable across multiple years, whereas in a common environment they were maintained at first but then progressively eroded. However, some epigenetic differentiation remained even after 10 asexual generations. Our data indicate that epigenetic variation in alligator weed most likely results from a combination of environmental induction and spontaneous epimutation, and that much of it is neither rapidly reversible (phenotypic plasticity) nor long-term stable, but instead displays an intermediate level of stability. Such transient epigenetic stability could be a beneficial mechanism in novel and heterogeneous environments, particularly in a genetically impoverished invader.

Differentially Expressed microRNAs and Target Genes Associated with Plastic Internode Elongation in Alternanthera philoxeroides in Contrasting Hydrological Habitats.

Phenotypic plasticity is crucial for plants to survive in changing environments. Discovering microRNAs, identifying their targets and further inferring microRNA functions in mediating plastic developmental responses to environmental changes have been a critical strategy for understanding the underlying molecular mechanisms of phenotypic plasticity. In this study, the dynamic expression patterns of microRNAs under contrasting hydrological habitats in the amphibious species Alternanthera philoxeroides were identified by time course expression profiling using high-throughput sequencing technology. A total of 128 known and 18 novel microRNAs were found to be differentially expressed under contrasting hydrological habitats. The microRNA:mRNA pairs potentially associated with plastic internode elongation were identified by integrative analysis of microRNA and mRNA expression profiles, and were validated by qRT-PCR and 5' RLM-RACE. The results showed that both the universal microRNAs conserved across different plants and the unique microRNAs novelly identified in A. philoxeroides were involved in the responses to varied water regimes. The results also showed that most of the differentially expressed microRNAs were transiently up-/down-regulated at certain time points during the treatments. The fine-scale temporal changes in microRNA expression highlighted the importance of time-series sampling in identifying stress-responsive microRNAs and analyzing their role in stress response/tolerance.

Gene Expression Reaction Norms Unravel the Molecular and Cellular Processes Underpinning the Plastic Phenotypes of Alternanthera Philoxeroides in Contrasting Hydrological Conditions.

Alternanthera philoxeroides is an amphibious invasive weed that can colonize both aquatic and terrestrial habitats. Individuals growing in different habitats exhibit extensive phenotypic variation but little genetic differentiation. Little is known about the molecular basis underlying environment-induced phenotypic changes. Variation in transcript abundance in A. philoxeroides was characterized throughout the time-courses of pond and upland treatments using RNA-Sequencing. Seven thousand eight hundred and five genes demonstrated variable expression in response to different treatments, forming 11 transcriptionally coordinated gene groups. Functional enrichment analysis of plastically expressed genes revealed pathway changes in hormone-mediated signaling, osmotic adjustment, cell wall remodeling, and programmed cell death, providing a mechanistic understanding of the biological processes underlying the phenotypic changes in A. philoxeroides. Both transcriptional modulation of environmentally sensitive loci and environmentally dependent control of regulatory loci influenced the plastic responses to the environment. Phenotypic responses and gene expression patterns to contrasting hydrological conditions were compared between A. philoxeroides and its alien congener Alternanthera pungens. The terricolous A. pungens displayed limited phenotypic plasticity to different treatments. It was postulated based on gene expression comparison that the interspecific variation in plasticity between A. philoxeroides and A. pungens was not due to environmentally-mediated changes in hormone levels but to variations in the type and relative abundance of different signal transducers and receptors expressed in the target tissue.

Extensive Transcriptome Changes Underlying the Flower Color Intensity Variation in Paeonia ostii.

Tree peonies are a group of traditional ornamental plants, especially in East Asia, with Paeonia ostii as one of the most important ancestral species. P. ostii has flowers with varying colors, ranging from nearly white, light pink to deep pink. However, few studies have been done to unravel the molecular mechanisms underlying the flower color intensity variation in plants. Based on comparative analyses of the pigment composition and transcriptomes of P. ostii with different flower color intensities, we found that the anthocyanin concentration was significantly correlated with the flower color intensity in P. ostii. Transcriptome analysis by RNA-Sequencing revealed 7187 genes that were differentially expressed between flowers with different color intensities. Functional enrichment analysis of differentially expressed genes revealed multiple pathways possibly responsible for color intensity variation in P. ostii, including flavonoid biosynthesis, fatty acid oxidation, carbohydrate metabolism, and hormone-mediated signaling. Particularly, while anthocyanin biosynthesis genes showing positive correlations between their expression and anthocyanin concentration in flowers, two transcription factors, PoMYB2 and PoSPL1, seem to negatively regulate anthocyanin accumulation by affecting the activation capacity of the MYB-bHLH-WDR complex, exhibiting an inverse relationship between their expression and anthocyanin accumulation. Our results showed that, although anthocyanin biosynthesis had a direct effect on the pigmentation of the P. ostii flower, other metabolic and hormone-mediated signaling pathways were also contributed to the flower color intensity variation in P. ostii, suggesting complex coordinated changes in the transcriptional network. Differential expression of genes encoding anthocyanin repressors seems to be the major factor responsible for the intensity variation in anthocyanin pigmentation in P. ostii.

Spatial genetic structure in natural populations of Phragmites australis in a mosaic of saline habitats in the Yellow River Delta, China.

Determination of spatial genetic structure (SGS) in natural populations is important for both theoretical aspects of evolutionary genetics and their application in species conservation and ecological restoration. In this study, we examined genetic diversity within and among the natural populations of a cosmopolitan grass Phragmites australis (common reed) in the Yellow River Delta (YRD), China, where a mosaic of habitat patches varying in soil salinity was detected. We demonstrated that, despite their close geographic proximity, the common reed populations in the YRD significantly diverged at six microsatellite loci, exhibiting a strong association of genetic variation with habitat heterogeneity. Genetic distances among populations were best explained as a function of environmental difference, rather than geographical distance. Although the level of genetic divergence among populations was relatively low (F'(ST) =0.073), weak but significant genetic differentiation, as well as the concordance between ecological and genetic landscapes, suggests spatial structuring of genotypes in relation to patchy habitats. These findings not only provided insights into the population dynamics of common reed in changing environments, but also demonstrated the feasibility of using habitat patches in a mosaic landscape as test systems to identify appropriate genetic sources for ecological restoration.

Genome-wide DNA methylation alterations of Alternanthera philoxeroides in natural and manipulated habitats: implications for epigenetic regulation of rapid responses to environmental fluctuation and phenotypic variation.

Alternanthera philoxeroides (alligator weed) is an invasive weed that can colonize both aquatic and terrestrial habitats. Individuals growing in different habitats exhibit extensive phenotypic variation but little genetic differentiation in its introduced range. The mechanisms underpinning the wide range of phenotypic variation and rapid adaptation to novel and changing environments remain uncharacterized. In this study, we examined the epigenetic variation and its correlation with phenotypic variation in plants exposed to natural and manipulated environmental variability. Genome-wide methylation profiling using methylation-sensitive amplified fragment length polymorphism (MSAP) revealed considerable DNA methylation polymorphisms within and between natural populations. Plants of different source populations not only underwent significant morphological changes in common garden environments, but also underwent a genome-wide epigenetic reprogramming in response to different treatments. Methylation alterations associated with response to different water availability were detected in 78.2% (169/216) of common garden induced polymorphic sites, demonstrating the environmental sensitivity and flexibility of the epigenetic regulatory system. These data provide evidence of the correlation between epigenetic reprogramming and the reversible phenotypic response of alligator weed to particular environmental factors.