Jingping Li

Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres

Polyploidy often confers emergent properties, such as the higher fibre productivity and quality of tetraploid cottons than diploid cottons bred for the same environments. Here we show that an abrupt five- to sixfold ploidy increase approximately 60 million years (Myr) ago, and allopolyploidy reuniting divergent Gossypium genomes approximately 1–2 Myr ago, conferred about 30–36-fold duplication of ancestral angiosperm (flowering plant) genes in elite cottons (Gossypium hirsutum and Gossypium barbadense), genetic complexity equalled only by Brassica among sequenced angiosperms. Nascent fibre evolution, before allopolyploidy, is elucidated by comparison of spinnable-fibred Gossypium herbaceum A and non-spinnable Gossypium longicalyx F genomes to one another and the outgroup D genome of non-spinnable Gossypium raimondii. The sequence of a G. hirsutum AtDt (in which ‘t’ indicates tetraploid) cultivar reveals many non-reciprocal DNA exchanges between subgenomes that may have contributed to phenotypic innovation and/or other emergent properties such as ecological adaptation by polyploids. Most DNA-level novelty in G. hirsutum recombines alleles from the D-genome progenitor native to its New World habitat and the Old World A-genome progenitor in which spinnable fibre evolved. Coordinated expression changes in proximal groups of functionally distinct genes, including a nuclear mitochondrial DNA block, may account for clusters of cotton-fibre quantitative trait loci affecting diverse traits. Opportunities abound for dissecting emergent properties of other polyploids, particularly angiosperms, by comparison to diploid progenitors and outgroups.

MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity

MCScan is an algorithm able to scan multiple genomes or subgenomes in order to identify putative homologous chromosomal regions, and align these regions using genes as anchors. The MCScanX toolkit implements an adjusted MCScan algorithm for detection of synteny and collinearity that extends the original software by incorporating 14 utility programs for visualization of results and additional downstream analyses. Applications of MCScanX to several sequenced plant genomes and gene families are shown as examples. MCScanX can be used to effectively analyze chromosome structural changes, and reveal the history of gene family expansions that might contribute to the adaptation of lineages and taxa. An integrated view of various modes of gene duplication can supplement the traditional gene tree analysis in specific families. The source code and documentation of MCScanX are freely available at http://chibba.pgml.uga.edu/mcscan2/.

The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes

Polyploidization has provided much genetic variation for plant adaptive evolution, but the mechanisms by which the molecular evolution of polyploid genomes establishes genetic architecture underlying species differentiation are unclear. Brassica is an ideal model to increase knowledge of polyploid evolution. Here we describe a draft genome sequence of Brassica oleracea, comparing it with that of its sister species B. rapa to reveal numerous chromosome rearrangements and asymmetrical gene loss in duplicated genomic blocks, asymmetrical amplification of transposable elements, differential gene co-retention for specific pathways and variation in gene expression, including alternative splicing, among a large number of paralogous and orthologous genes. Genes related to the production of anticancer phytochemicals and morphological variations illustrate consequences of genome duplication and gene divergence, imparting biochemical and morphological variation to B. oleracea. This study provides insights into Brassica genome evolution and will underpin research into the many important crops in this genus.

Convergent evolution of perenniality in rice and sorghum

Annual and perennial habit are two major strategies by which grasses adapt to seasonal environmental change, and these distinguish cultivated cereals from their wild relatives. Rhizomatousness, a key trait contributing to perenniality, was investigated by using an F2 population from a cross between cultivated rice (Oryza sativa) and its wild relative, Oryza longistaminata. Molecular mapping based on a complete simple sequence-repeat map revealed two dominant-complementary genes controlling rhizomatousness. Rhz3 was mapped to the interval between markers OSR16 [1.3 centimorgans (cM)] and OSR13 (8.1 cM) on rice chromosome 4 and Rhz2 located between RM119 (2.2 cM) and RM273 (7.4 cM) on chromosome 3. Comparative mapping indicated that each gene closely corresponds to major quantitative trait loci (QTLs) controlling rhizomatousness in Sorghum propinquum, a wild relative of cultivated sorghum. Correspondence of these genes in rice and sorghum, which diverged from a common ancestor ≈50 million years ago, suggests that the two genes may be key regulators of rhizome development in many Poaceae. Many additional QTLs affecting abundance of rhizomes in O. longistaminata were identified, most of which also corresponded to the locations of S. propinquum QTLs. Convergent evolution of independent mutations at, in some cases, corresponding genes may have been responsible for the evolution of annual cereals from perennial wild grasses. DNA markers closely linked to Rhz2 and Rhz3 will facilitate cloning of the genes, which may contribute significantly to our understanding of grass evolution, advance opportunities to develop perennial cereals, and offer insights into environmentally benign weed-control strategies.

Integrated Syntenic and Phylogenomic Analyses Reveal an Ancient Genome Duplication in Monocots

Whole-genome duplication (WGD) is a primary source of genetic material for evolutionary variation. This work compares the genomes of four monocots and two eudicots using integrated phylogenomic and syntenic analyses, revealing an ancient WGD that shaped the genomes of all commelinid monocots, including grasses, bromeliads, bananas, gingers, palms, and other economically important plants. Unraveling widespread polyploidy events throughout plant evolution is a necessity for inferring the impacts of whole-genome duplication (WGD) on speciation, functional innovations, and to guide identification of true orthologs in divergent taxa. Here, we employed an integrated syntenic and phylogenomic analyses to reveal an ancient WGD that shaped the genomes of all commelinid monocots, including grasses, bromeliads, bananas (Musa acuminata), ginger, palms, and other plants of fundamental, agricultural, and/or horticultural interest. First, comprehensive phylogenomic analyses revealed 1421 putative gene families that retained ancient duplication shared by Musa (Zingiberales) and grass (Poales) genomes, indicating an ancient WGD in monocots. Intergenomic synteny blocks of Musa and Oryza were investigated, and 30 blocks were shown to be duplicated before Musa-Oryza divergence an estimated 120 to 150 million years ago. Synteny comparisons of four monocot (rice [Oryza sativa], sorghum [Sorghum bicolor], banana, and oil palm [Elaeis guineensis]) and two eudicot (grape [Vitis vinifera] and sacred lotus [Nelumbo nucifera]) genomes also support this additional WGD in monocots, herein called Tau (τ). Integrating synteny and phylogenomic comparisons achieves better resolution of ancient polyploidy events than either approach individually, a principle that is exemplified in the disambiguation of a WGD series of rho (ρ)-sigma (σ)-tau (τ) in the grass lineages that echoes the alpha (α)-beta (β)-gamma (γ) series previously revealed in the Arabidopsis thaliana lineage.

Comparative analysis of peanut NBS‐LRR gene clusters suggests evolutionary innovation among duplicated domains and erosion of gene microsynteny

• Plant genomes contain numerous disease resistance genes (R genes) that play roles in defense against pathogens. Scarcity of genetic polymorphism makes peanut (Arachis hypogaea) especially vulnerable to a wide variety of pathogens. • Here, we isolated and characterized peanut bacterial artificial chromosomes (BACs) containing a high density of R genes. Analysis of two genomic regions identified several TIR-NBS-LRR (Toll-interleukin-1 receptor, nucleotide-binding site, leucine-rich repeat) resistance gene analogs or gene fragments. We reconstructed their evolutionary history characterized by tandem duplications, possibly facilitated by transposon activities. We found evidence of both intergenic and intragenic gene conversions and unequal crossing-over, which may be driving forces underlying the functional evolution of resistance. • Analysis of the sequence mutations, protein secondary structure and three-dimensional structures, all suggest that LRR domains are the primary contributor to the evolution of resistance genes. The central part of LRR regions, assumed to serve as the active core, may play a key role in the resistance function by having higher rates of duplication and DNA conversion than neighboring regions. The assumed active core is characterized by significantly enriched leucine residue composition, accumulation of positively selected sites, and shorter beta sheets. • Homologous resistance gene analog (RGA)-containing regions in peanut, soybean, Medicago, Arabidopsis and grape have only limited gene synteny and microcollinearity.

CSGRqtl, a Comparative Quantitative Trait Locus Database for Saccharinae Grasses

Summary: By aligning QTLs from many populations and several species, this study increases knowledge of the genetic control of agriculturally and developmentally important traits in the Saccharinae clade of grasses, expedites translation of knowledge from better-studied to less-studied species, and facilitates investigation of fundamental questions across the genomes and paleoduplicated “subgenomes” of divergent taxa.

Comparative Genetics of Seed Size Traits in Divergent Cereal Lineages Represented by Sorghum (Panicoidae) and Rice (Oryzoidae)

Seed size is closely related to fitness of wild plants, and its modification has been a key recurring element in domestication of seed/grain crops. In sorghum, a genomic and morphological model for panicoid cereals, a rich history of research into the genetics of seed size is reflected by a total of 13 likelihood intervals determined by conventional QTL (linkage) mapping in 11 nonoverlapping regions of the genome. To complement QTL data and investigate whether the discovery of seed size QTL is approaching “saturation,” we compared QTL data to GWAS for seed mass, seed length, and seed width studied in 354 accessions from a sorghum association panel (SAP) that have been genotyped at 265,487 SNPs. We identified nine independent GWAS-based “hotspots” for seed size associations. Targeted resequencing near four association peaks with the most notable linkage disequilibrium provides further support of the role(s) of these regions in the genetic control of sorghum seed size and identifies two candidate causal variants with nonsynonymous mutations. Of nine GWAS hotspots in sorghum, seven have significant correspondence with rice QTL intervals and known genes for components of seed size on orthologous chromosomes. Identifying intersections between positional and association genetic data are a potentially powerful means to mitigate constraints associated with each approach, and nonrandom correspondence of sorghum (panicoid) GWAS signals to rice (oryzoid) QTL adds a new dimension to the ability to leverage genetic data about this important trait across divergent plants.

Ancient and Recent Polyploidy in Monocots

At least two whole-genome duplications (WGD) have profoundly influenced the evolution of most, if not all, grass (Poaceae) genomes, with the most recent of these predating the divergence of these lineages by 20 million or more years. Taxa within each major lineage of Poaceae (e.g., Panicoideae, Ehrhartoideae, Pooideae) have independently experienced additional polyploidizations that have been of central importance to the evolution and productivity of some of our most important crop plants [for example, sugarcane (Saccharum spp.), and durum and bread wheat (Triticum spp.)]. Following polyploidy, adaptation to the duplicated state is evident at the levels of transmission genetics, chromosome structure, and gene repertoire. While most duplicated chromosomal regions re-establish largely independent evolution within a few million years, 70-million-year-old duplicated chromosome segments in one unusual region of the rice genome and its orthologs in other grasses have continued to exhibit concerted evolution more recently than the divergence of rice subspecies japonica and indica an estimated 400,000 years ago.

Comparative and Evolutionary Analysis of Major Peanut Allergen Gene Families

Peanut (Arachis hypogaea L.) causes one of the most serious food allergies. Peanut seed proteins, Arah1, Arah2, and Arah3, are considered to be among the most important peanut allergens. To gain insights into genome organization and evolution of allergen-encoding genes, approximately 617 kb from the genome of cultivated peanut and 215 kb from a wild relative were sequenced including three Arah1, one Arah2, eight Arah3, and two Arah6 gene family members. To assign polarity to differences between homoeologous regions in peanut, we used as outgroups the single orthologous regions in Medicago, Lotus, common bean, chickpea, and pigeonpea, which diverged from peanut about 50 Ma and have not undergone subsequent polyploidy. These regions were also compared with orthologs in many additional dicot plant species to help clarify the timing of evolutionary events. The lack of conservation of allergenic epitopes between species, and the fact that many different proteins can be allergenic, makes the identification of allergens across species by comparative studies difficult. The peanut allergen genes are interspersed with low-copy genes and transposable elements. Phylogenetic analyses revealed lineage-specific expansion and loss of low-copy genes between species and homoeologs. Arah1 syntenic regions are conserved in soybean, pigeonpea, tomato, grape, Lotus, and Arabidopsis, whereas Arah3 syntenic regions show genome rearrangements. We infer that tandem and segmental duplications led to the establishment of the Arah3 gene family. Our analysis indicates differences in conserved motifs in allergen proteins and in the promoter regions of the allergen-encoding genes. Phylogenetic analysis and genomic organization studies provide new insights into the evolution of the major peanut allergen-encoding genes.