Intertwined signatures of desiccation and drought tolerance in grasses.

Grasses are among the most resilient plants, and some can survive prolonged desiccation in semiarid regions with seasonal rainfall. However, the genetic elements that distinguish grasses that are sensitive versus tolerant to extreme drying are largely unknown. Here, we leveraged comparative genomic approaches with the desiccation-tolerant grass Eragrostis nindensis and the related desiccation-sensitive cereal Eragrostis tef to identify changes underlying desiccation tolerance. These analyses were extended across C4 grasses and cereals to identify broader evolutionary conservation and divergence. Across diverse genomic datasets, we identified changes in chromatin architecture, methylation, gene duplications, and expression dynamics related to desiccation in E. nindensis It was previously hypothesized that transcriptional rewiring of seed desiccation pathways confers vegetative desiccation tolerance. Here, we demonstrate that the majority of seed-dehydration-related genes showed similar expression patterns in leaves of both desiccation-tolerant and -sensitive species. However, we identified a small set of seed-related orthologs with expression specific to desiccation-tolerant species. This supports a broad role for seed-related genes, where many are involved in typical drought responses, with only a small subset of crucial genes specifically induced in desiccation-tolerant plants.

Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff.

Teff (Eragrostis tef) is a cornerstone of food security in the Horn of Africa, where it is prized for stress resilience, grain nutrition, and market value. Here, we report a chromosome-scale assembly of allotetraploid teff (variety Dabbi) and patterns of subgenome dynamics. The teff genome contains two complete sets of homoeologous chromosomes, with most genes maintaining as syntenic gene pairs. TE analysis allows us to estimate that the teff polyploidy event occurred ~1.1 million years ago (mya) and that the two subgenomes diverged ~5.0 mya. Despite this divergence, we detect no large-scale structural rearrangements, homoeologous exchanges, or biased gene loss, in contrast to many other allopolyploids. The two teff subgenomes have partitioned their ancestral functions based on divergent expression across a diverse expression atlas. Together, these genomic resources will be useful for accelerating breeding of this underutilized grain crop and for fundamental insights into polyploid genome evolution.

Fusarium virguliform e Transcriptional Plasticity Is Revealed by Host Colonization of Maize versus Soybean.

We exploited the broad host range of Fusarium virguliforme to identify differential fungal responses leading to either an endophytic or a pathogenic lifestyle during colonization of maize (Zea mays) and soybean (Glycine max), respectively. To provide a foundation to survey the transcriptomic landscape, we produced an improved de novo genome assembly and annotation of F. virguliforme using PacBio sequencing. Next, we conducted a high-resolution time course of F. virguliforme colonization and infection of both soybean, a symptomatic host, and maize, an asymptomatic host. Comparative transcriptomic analyses uncovered a nearly complete network rewiring, with less than 8% average gene coexpression module overlap upon colonizing the different plant hosts. Divergence of transcriptomes originating from host specific temporal induction genes is central to infection and colonization, including carbohydrate-active enzymes (CAZymes) and necrosis inducing effectors. Upregulation of Zn(II)-Cys6 transcription factors were uniquely induced in soybean at 2 d postinoculation, suggestive of enhanced pathogen virulence on soybean. In total, the data described herein suggest that F. virguliforme modulates divergent infection profiles through transcriptional plasticity.

Massive Tandem Proliferation of ELIPs Supports Convergent Evolution of Desiccation Tolerance across Land Plants.

Desiccation tolerance was a critical adaptation for the colonization of land by early nonvascular plants. Resurrection plants have maintained or rewired these ancestral protective mechanisms, and desiccation-tolerant species are dispersed across the land plant phylogeny. Although common physiological, biochemical, and molecular signatures are observed across resurrection plant lineages, features underlying the recurrent evolution of desiccation tolerance are unknown. Here we used a comparative approach to identify patterns of genome evolution and gene duplication associated with desiccation tolerance. We identified a single gene family with dramatic expansion in all sequenced resurrection plant genomes and no expansion in desiccation-sensitive species. This gene family of early light-induced proteins (ELIPs) expanded in resurrection plants convergent through repeated tandem gene duplication. ELIPs are universally highly expressed during desiccation in all surveyed resurrection plants and may play a role in protecting against photooxidative damage of the photosynthetic apparatus during prolonged dehydration. Photosynthesis is particularly sensitive to dehydration, and the increased abundance of ELIPs may help facilitate the rapid recovery observed for most resurrection plants. Together, these observations support convergent evolution of desiccation tolerance in land plants through tandem gene duplication.

Desiccation Tolerance Evolved through Gene Duplication and Network Rewiring in Lindernia.

Although several resurrection plant genomes have been sequenced, the lack of suitable dehydration-sensitive outgroups has limited genomic insights into the origin of desiccation tolerance. Here, we utilized a comparative system of closely related desiccation-tolerant (Lindernia brevidens) and -sensitive (Lindernia subracemosa) species to identify gene- and pathway-level changes associated with the evolution of desiccation tolerance. The two high-quality Lindernia genomes we assembled are largely collinear, and over 90% of genes are conserved. L. brevidens and L. subracemosa have evidence of an ancient, shared whole-genome duplication event, and retained genes have neofunctionalized, with desiccation-specific expression in L. brevidens Tandem gene duplicates also are enriched in desiccation-associated functions, including a dramatic expansion of early light-induced proteins from 4 to 26 copies in L. brevidens A comparative differential gene coexpression analysis between L. brevidens and L. subracemosa supports extensive network rewiring across early dehydration, desiccation, and rehydration time courses. Many LATE EMBRYOGENESIS ABUNDANT genes show significantly higher expression in L. brevidens compared with their orthologs in L. subracemosa Coexpression modules uniquely upregulated during desiccation in L. brevidens are enriched with seed-specific and abscisic acid-associated cis-regulatory elements. These modules contain a wide array of seed-associated genes that have no expression in the desiccation-sensitive L. subracemosa Together, these findings suggest that desiccation tolerance evolved through a combination of gene duplications and network-level rewiring of existing seed desiccation pathways.

The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism.

Crassulacean acid metabolism (CAM) is a water-use efficient adaptation of photosynthesis that has evolved independently many times in diverse lineages of flowering plants. We hypothesize that convergent evolution of protein sequence and temporal gene expression underpins the independent emergences of CAM from C3 photosynthesis. To test this hypothesis, we generate a de novo genome assembly and genome-wide transcript expression data for Kalanchoë fedtschenkoi, an obligate CAM species within the core eudicots with a relatively small genome (~260 Mb). Our comparative analyses identify signatures of convergence in protein sequence and re-scheduling of diel transcript expression of genes involved in nocturnal CO2 fixation, stomatal movement, heat tolerance, circadian clock, and carbohydrate metabolism in K. fedtschenkoi and other CAM species in comparison with non-CAM species. These findings provide new insights into molecular convergence and building blocks of CAM and will facilitate CAM-into-C3 photosynthesis engineering to enhance water-use efficiency in crops.

Assembling allopolyploid genomes: no longer formidable.

A combined approach of whole genome shotgun sequencing and ultra-high density linkage mapping using skim sequencing of a segregating population is effective for assembling allopolyploid genomes.