Evolution

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    Incomplete reproductive isolation between Rhododendron taxa enables hybrid formation and persistence
    Li-Jun Yan, Kevin S. Burgess, Wei Zheng, Zhi-Bin Tao, De-Zhu Li and Lian-Ming Gao
    J Integr Plant Biol 2019, 61 (4): 433-448.  
    DOI: 10.1111/jipb.12718
    Abstract (Browse 217)  |   Save
    The evolutionary consequences of hybridization ultimately depend on the magnitude of reproductive isolation between hybrids and their parents. We evaluated the relative contributions of pre- and post-zygotic barriers to reproduction for hybrid formation, hybrid persistence and potential for reproductive isolation of hybrids formed between two Rhododendron species, R. spiciferum and R. spinuliferum. Our study established that incomplete reproductive isolation promotes hybrid formation and persistence and delays hybrid speciation. All pre-zygotic barriers to reproduction leading to hybrid formation are incomplete: parental species have overlapping flowering; they share the same pollinators; reciprocal assessments of pollen tube germination and growth do not differ among parents. The absence of post-zygotic barriers between parental taxa indicates that the persistence of hybrids is likely. Reproductive isolation was incomplete between hybrids and parents in all cases studied, although asymmetric differences in reproductive fitness were prevalent and possibly explain the genetic structure of natural hybrid swarms where hybridization is known to be bidirectional but asymmetric. Introgression, rather than speciation, is a probable evolutionary outcome of hybridization between the two Rhododendron taxa. Our study provides insights into understanding the evolutionary implications of natural hybridization in woody plants.
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    Domestication and crop evolution of wheat and barley: Genes, genomics, and future directions
    Matthew Haas, Mona Schreiber and Martin Mascher
    J Integr Plant Biol 2019, 61 (3): 204-225.  
    doi: 10.1111/jipb.12737
    Abstract (Browse 220)  |   Save
    Wheat and barley are two of the founder crops of the agricultural revolution that took place 10,000 years ago in the Fertile Crescent and both crops remain among the world's most important crops. Domestication of these crops from their wild ancestors required the evolution of traits useful to humans, rather than survival in their natural environment. Of these traits, grain retention and threshability, yield improvement, changes to photoperiod sensitivity and nutritional value are most pronounced between wild and domesticated forms. Knowledge about the geographical origins of these crops and the genes responsible for domestication traits largely pre-dates the era of next-generation sequencing, although sequencing will lead to new insights. Molecular markers were initially used to calculate distance (relatedness), genetic diversity and to generate genetic maps which were useful in cloning major domestication genes. Both crops are characterized by large, complex genomes which were long thought to be beyond the scope of whole-genome sequencing. However, advances in sequencing technologies have improved the state of genomic resources for both wheat and barley. The availability of reference genomes for wheat and some of its progenitors, as well as for barley, sets the stage for answering unresolved questions in domestication genomics of wheat and barley.
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    Analysis of the chromatin binding affinity of retrotransposases reveals novel roles in diploid and tetraploid cotton
    Jing Lin, Ying Cai, Gai Huang, Yan Yang, Yang Li, Kun Wang and Zhiguo Wu
    J Integr Plant Biol 2019, 61 (1): 32-44.  
    doi: 10.1111/jipb.12740
    Abstract (Browse 335)  |   Save
    LTR-retrotransposable elements are major components of diploid (Gossypium arboreum) and tetraploid (Gossypium hirsutum) cotton genomes that have undergone dramatic increases in copy number during the course of evolution. However, little is known about the biological functions of LTR-retrotransposable elements in cotton. Here, we show that a copia-like LTR-retrotransposable element has maintained considerable activity in both G. arboreum and G. hirsutum. We identified two functional domains of the retrotransposon and analyzed their expression levels in various cotton tissues, including leaves, ovules, and germinating seeds. ChIP-qPCR (chromatin immunoprecipitation followed by quantitative PCR), using a copia-specific antibody, established that copia-like proteins primarily bind to the first exons of several protein-coding genes in cotton cells. This finding suggests that retrotransposons play a novel, important role in regulating the transcriptional activities of protein-coding genes with various biological activities.
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    A Malvaceae mystery: A mallow maelstrom of genome multiplications and maybe misleading methods?
    Justin L. Conover, Nisa Karimi, Noah Stenz, Cécile Ané, Corrinne E. Grover, Cynthia Skema, Jennifer A. Tate, Kirsten Wolff, Samuel A. Logan, Jonathan F. Wendel and David A. Baum
    J Integr Plant Biol 2019, 61 (1): 12-31.  
    doi: 10.1111/jipb.12746
    Abstract (Browse 252)  |   Save
    Previous research suggests that Gossypium has undergone a 5- to 6-fold multiplication following its divergence from Theobroma. However, the number of events, or where they occurred in the Malvaceae phylogeny remains unknown. We analyzed transcriptomic and genomic data from representatives of eight of the nine Malvaceae subfamilies. Phylogenetic analysis of nuclear data placed Dombeya (Dombeyoideae) as sister to the rest of Malvadendrina clade, but the plastid DNA tree strongly supported Durio (Helicteroideae) in this position. Intraspecific Ks plots indicated that all sampled taxa, except Theobroma (Byttnerioideae), Corchorus (Grewioideae), and Dombeya (Dombeyoideae), have experienced whole genome multiplications (WGMs). Quartet analysis suggested WGMs were shared by Malvoideae-Bombacoideae and Sterculioideae-Tilioideae, but did not resolve whether these are shared with each other or Helicteroideae (Durio). Gene tree reconciliation and Bayesian concordance analysis suggested a complex history. Alternative hypotheses are suggested, each involving two independent autotetraploid and one allopolyploid event. They differ in that one entails an allopolyploid origin for the Durio lineage, whereas the other invokes an allopolyploid origin for Malvoideae-Bombacoideae. We highlight the need for more genomic information in the Malvaceae and improved methods to resolve complex evolutionary histories that may include allopolyploidy, incomplete lineage sorting, and variable rates of gene and genome evolution.
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    Functional diversifications of GhERF1 duplicate genes after the formation of allotetraploid cotton
    Chunxiao Liu and TianZhen Zhang
    J Integr Plant Biol 2019, 61 (1): 60-74.  
    doi: 10.1111/jipb.12764
    Abstract (Browse 210)  |   Save
    Whole genome duplication, a prevalent force of evolution in plants, results in massive genome restructuring in different organisms. Roles of the resultant duplicated genes are poorly understood, both functionally and evolutionarily. In the present study, differentially expressed ethylene responsive factors (GhERF1s), anchored on Chr-A07 and Chr-D07, were isolated from a high-yielding cotton hybrid (XZM2) and its parents. The GhERF1 was located in the B3 subgroup of the ethylene responsive factors subfamily involved in conferring tolerance to abiotic stress. Nucleotide sequence analysis of 524 diverse accessions, together with quantitative real-time polymerase chain reaction analysis, elucidated that de-functionalization of GhERF1-7A occurred due to one base insertion following formation of the allotetraploid cotton. Our quantitative trait loci and association mapping analyses highlighted a role for GhERF1-7A in conferring high boll number per plant in modern cotton cultivars. Overexpression of GhERF1-7A in transgenic Arabidopsis resulted in a substantial increase in the number of siliques and total seed yield. Neo-functionalization of GhERF1-7A was also observed in modern cultivars rather than in races and/or landraces, further supporting its role in the development of high-yielding cotton cultivars. Both de- and neo-functionalization occurred in one of the duplicate genes, thus providing new genomic insight into the evolution of allotetraploid cotton species.
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    Recurrent genome duplication events likely contributed to both the ancient and recent rise of ferns
    Chien-Hsun Huang, Xinping Qi, Duoyuan Chen, Ji Qi and Hong Ma
    J Integr Plant Biol 2020, 62 (4): 433-455.  
    doi: 10.1111/jipb.12877
    Abstract (Browse 436)  |   Save

    Ferns, the second largest group of vascular plants, originated ~400 million years ago (Mya). They became dominant in the ancient Earth landscape before the angiosperms and are still important in current ecosystems. Many ferns have exceptionally high chromosome numbers, possibly resulting from whole‐genome duplications (WGDs). However, WGDs have not been investigated molecularly across fern diversity. Here we detected and dated fern WGDs using a phylogenomic approach and by calculating synonymous substitution rates (Ks). We also investigated a possible correlation between proposed WGDs and shifts in species diversification rates. We identified 19 WGDs: three ancient events along the fern phylogenetic backbone that are shared by 66%–97% of extant ferns, with additional lineage‐specific WGDs for eight orders, providing strong evidence for recurring genome duplications across fern evolutionary history. We also observed similar Ks peak values for more than half of these WGDs, with multiple WGDs occurring close to the Cretaceous (~145–66 Mya). Despite the repeated WGD events, the biodiversity of ferns declined during the Cretaceous, implying that other factors probably contributed to the floristic turnover from ferns to angiosperms. This study provides molecular evidence for recurring WGDs in ferns and offers important clues to the genomic evolutionary history of ferns.

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    The origin of Wxla provides new insights into the improvement of grain quality in rice
    Hao Zhou, Duo Xia, Da Zhao, Yanhua Li, Pingbo Li, Bian Wu, Guanjun Gao, Qinglu Zhang, Gongwei Wang, Jinghua Xiao, Xianghua Li, Sibin Yu, Xingming Lian and Yuqing He
    J Integr Plant Biol 2021, 63 (5): 878-888.  
    doi: 10.1111/jipb.13011
    Abstract (Browse 459)  |   Save
    Appearance and taste are important factors in rice (Oryza sativa) grain quality. Here, we investigated the taste scores and related eating‐quality traits of 533 diverse cultivars to assess the relationships between—and genetic basis of—rice taste and eating‐quality. A genome‐wide association study highlighted the Wx gene as the major factor underlying variation in taste and eating quality. Notably, a novel waxy (Wx) allele, Wxla, which combined two mutations from Wxb and Wxin, exhibited a unique phenotype. Reduced GBSSI activity conferred Wxla rice with both a transparent appearance and good eating quality. Haplotype analysis revealed that Wxla was derived from intragenic recombination. In fact, the recombination rate at the Wx locus was estimated to be 3.34 kb/cM, which was about 75‐fold higher than the genome‐wide mean, indicating that intragenic recombination is a major force driving diversity at the Wx locus. Based on our results, we propose a new network for Wx evolution, noting that new Wx alleles could easily be generated by crossing genotypes with different Wx alleles. This study thus provides insights into the evolution of the Wx locus and facilitates molecular breeding for quality in rice.
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    Contribution of phenylpropanoid metabolism to plant development and plant–environment interactions
    Nai-Qian Dong and Hong-Xuan Lin
    J Integr Plant Biol 2021, 63 (1): 180-209.  
    doi: 10.1111/jipb.13054
    Abstract (Browse 729)  |   Save
    Phenylpropanoid metabolism is one of the most important metabolisms in plants, yielding more than 8,000 metabolites contributing to plant development and plant–environment interplay. Phenylpropanoid metabolism materialized during the evolution of early freshwater algae that were initiating terrestrialization and land plants have evolved multiple branches of this pathway, which give rise to metabolites including lignin, flavonoids, lignans, phenylpropanoid esters, hydroxycinnamic acid amides, and sporopollenin. Recent studies have revealed that many factors participate in the regulation of phenylpropanoid metabolism, and modulate phenylpropanoid homeostasis when plants undergo successive developmental processes and are subjected to stressful environments. In this review, we summarize recent progress on elucidating the contribution of phenylpropanoid metabolism to the coordination of plant development and plant–environment interaction, and metabolic flux redirection among diverse metabolic routes. In addition, our review focuses on the regulation of phenylpropanoid metabolism at the transcriptional, post‐transcriptional, post‐translational, and epigenetic levels, and in response to phytohormones and biotic and abiotic stresses.
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    An update on the function and regulation of methylerythritol phosphate and mevalonate pathways and their evolutionary dynamics
    Xiaojun Pu, Xiumei Dong, Qing Li, Zexi Chen and Li Liu
    J Integr Plant Biol 2021, 63 (7): 1211-1226.  
    DOI: 10.1111/jipb.13076
    Abstract (Browse 318)  |   Save
    Isoprenoids are among the largest and most chemically diverse classes of organic compounds in nature and are involved in the processes of photosynthesis, respiration, growth, development, and plant responses to stress. The basic building block units for isoprenoid synthesis—isopentenyl diphosphate and its isomer dimethylallyl diphosphate—are generated by the mevalonate (MVA) and methylerythritol phosphate (MEP) pathways. Here, we summarize recent advances on the roles of the MEP and MVA pathways in plant growth, development and stress responses, and attempt to define the underlying gene networks that orchestrate the MEP and MVA pathways in response to developmental or environmental cues. Through phylogenomic analysis, we also provide a new perspective on the evolution of the plant isoprenoid pathway. We conclude that the presence of the MVA pathway in plants may be associated with the transition from aquatic to subaerial and terrestrial environments, as lineages for its core components are absent in green algae. The emergence of the MVA pathway has acted as a key evolutionary event in plants that facilitated land colonization and subsequent embryo development, as well as adaptation to new and varied environments.
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    Phylotranscriptomic insights into Asteraceae diversity, polyploidy, and morphological innovation
    Caifei Zhang, Chien‐Hsun Huang, Mian Liu, Yi Hu, Jose L. Panero, Federico Luebert, Tiangang Gao and Hong Ma
    J Integr Plant Biol 2021, 63 (7): 1273-1293.  
    doi: 10.1111/jipb.13078
    Abstract (Browse 370)  |   Save
    Biodiversity is not evenly distributed among related groups, raising questions about the factors contributing to such disparities. The sunflower family (Asteraceae, >26,000 species) is among the largest and most diverse plant families, but its species diversity is concentrated in a few subfamilies, providing an opportunity to study the factors affecting biodiversity. Phylotranscriptomic analyses here of 244 transcriptomes and genomes produced a phylogeny with strong support for the monophyly of Asteraceae and the monophyly of most subfamilies and tribes. This phylogeny provides a reference for detecting changes in diversification rates and possible factors affecting Asteraceae diversity, which include global climate shifts, whole-genome duplications (WGDs), and morphological evolution. The origin of Asteraceae was estimated at ~83 Mya, with most subfamilies having diverged before the Cretaceous–Paleocene boundary. Phylotranscriptomic analyses supported the existence of 41 WGDs in Asteraceae. Changes to herbaceousness and capitulescence with multiple flower-like capitula, often with distinct florets and scaly pappus/receptacular bracts, are associated with multiple upshifts in diversification rate. WGDs might have contributed to the survival of early Asteraceae by providing new genetic materials to support morphological transitions. The resulting competitive advantage for adapting to different niches would have increased biodiversity in Asteraceae.
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    Insights into salvianolic acid B biosynthesis from chromosome-scale assembly of the Salvia bowleyana genome
    Xuehai Zheng, Duo Chen, Binghua Chen, Limin Liang, Zhen Huang, Wenfang Fan, Jiannan Chen, Wenjin He, Huibin Chen, Luqiang Huang, Youqiang Chen, Jinmao Zhu and Ting Xue
    J Integr Plant Biol 2021, 63 (7): 1309-1323.  
    DOI: 10.1111/jipb.13085
    Abstract (Browse 262)  |   Save
    Salvia bowleyana is a traditional Chinese medicinal plant that is a source of nutritional supplements rich in salvianolic acid B and a potential experimental system for the exploration of salvianolic acid B biosynthesis in the Labiatae. Here, we report a high-quality chromosome-scale genome assembly of S. bowleyana covering 462.44 Mb, with a scaffold N50 value of 57.96 Mb and 44,044 annotated protein-coding genes. Evolutionary analysis revealed an estimated divergence time between S. bowleyana and its close relative S. miltiorrhiza of ~3.94 million years. We also observed evidence of a whole-genome duplication in the S. bowleyana genome. Transcriptome analysis showed that SbPAL1 (PHENYLALANINE AMMONIA-LYASE1) is highly expressed in roots relative to stem and leaves, paralleling the location of salvianolic acid B accumulation. The laccase gene family in S. bowleyana outnumbered their counterparts in both S. miltiorrhiza and Arabidopsis thaliana, suggesting that the gene family has undergone expansion in S. bowleyana. Several laccase genes were also highly expressed in roots, where their encoded proteins may catalyze the oxidative reaction from rosmarinic acid to salvianolic acid B. These findings provide an invaluable genomic resource for understanding salvianolic acid B biosynthesis and its regulation, and will be useful for exploring the evolution of the Labiatae.
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    Balancing selection and wild gene pool contribute to resistance in global rice germplasm against planthopper
    Cong Zhou, Qian Zhang, Yu Chen, Jin Huang, Qin Guo, Yi Li, Wensheng Wang, Yongfu Qiu, Wei Guan, Jing Zhang, Jianping Guo, Shaojie Shi, Di Wu, Xiaohong Zheng, Lingyun Nie, Jiaoyan Tan, Chaomei Huang, Yinhua Ma, Fang Yang, Xiqin Fu, Bo Du, Lili Zhu, Rongzhi Chen, Zhikang Li, Longping Yuan and Guangcun He
    J Integr Plant Biol 2021, 63 (10): 1695-1711.  
    doi: 10.1111/jipb.13157
    Abstract (Browse 323)  |   Save
    Interactions and co-evolution between plants and herbivorous insects are critically important in agriculture. Brown planthopper (BPH) is the most severe insect of rice, and the biotypes adapt to feed on different rice genotypes. Here, we present genomics analyses on 1,520 global rice germplasms for resistance to three BPH biotypes. Genome-wide association studies identified 3,502 single nucleotide polymorphisms (SNPs) and 59 loci associated with BPH resistance in rice. We cloned a previously unidentified gene Bph37 that confers resistance to BPH. The associated loci showed high nucleotide diversity. Genome-wide scans for trans-species polymorphisms revealed ancient balancing selection at the loci. The secondarily evolved insect biotypes II and III exhibited significantly higher virulence and overcame more rice varieties than the primary biotype I. In response, more SNPs and loci evolved in rice for resistance to biotypes II and III. Notably, three exceptional large regions with high SNP density and resistance-associated loci on chromosomes 4 and 6 appear distinct between the resistant and susceptible rice varieties. Surprisingly, these regions in resistant rice might have been retained from wild species Oryza nivara. Our findings expand the understanding of long-term interactions between rice and BPH and provide resistance genes and germplasm resources for breeding durable BPH-resistant rice varieties.
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