Nuclear phylotranscriptomics and phylogenomics support numerous polyploidization events and hypotheses for the evolution of rhizobial nitrogen-fixing symbiosis in Fabaceae

Molecular Plant - Tập 14 - Trang 748-773 - 2021
Yiyong Zhao1,2, Rong Zhang3, Kai-Wen Jiang4,5, Ji Qi1, Yi Hu2, Jing Guo1, Renbin Zhu6, Taikui Zhang1, Ashley N. Egan7, Ting-Shuang Yi3, Chien-Hsun Huang1, Hong Ma2
1State Key Laboratory of Genetic Engineering and Collaborative Innovation Center of Genetics and Development, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, 2005 Songhu Road, Shanghai 200433, China
2Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA
3Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Lanhei Road, Kunming 650201, China
4Key Laboratory of Biodiversity Conservation in Southwest China, State Forestry Administration, Southwest Forestry University, Kunming 650224, PR China
5Ningbo Botanical Garden Herbarium, Ningbo 315201, PR China
6Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Yunnan 666303, PR China
7Department of Biology, Utah Valley University, Orem, UT, 84058, USA

Tài liệu tham khảo

Afkhami, 2018, Symbioses with nitrogen-fixing bacteria: nodulation and phylogenetic data across legume genera, Ecology, 99, 502, 10.1002/ecy.2110 Barker, 1990, Medicago truncatula, a model plant for studying the molecular genetics of the Rhizobium-legume symbiosis, Plant Mol. Biol. Rep., 8, 40, 10.1007/BF02668879 Battenberg, 2018, Comparative transcriptomic analysis of two actinorhizal plants and the legume Medicago truncatula supports the homology of root nodule symbioses and is congruent with a two-step process of evolution in the nitrogen-fixing clade of angiosperms, Front. Plant Sci., 9, 1256, 10.3389/fpls.2018.01256 Beaulieu, 2013, Identifying hidden rate changes in the evolution of a binary morphological character: the evolution of plant habit in Campanulid angiosperms, Syst. Biol., 62, 725, 10.1093/sysbio/syt034 Beerling, 2011, Convergent cenozoic CO2 history, Nat. Geosci., 4, 418, 10.1038/ngeo1186 Bell, 1981, Non-protein amino acids in the Leguminosae, 489 Benton, 2010, The origins of modern biodiversity on land, Philos. Trans. R. Soc. Lond. Ser. B: Biol. Sci., 365, 3667, 10.1098/rstb.2010.0269 Bertioli, 2016, The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut, Nat. Genet., 48, 438, 10.1038/ng.3517 Birky, 2001, The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models, Annu. Rev. Genet., 35, 125, 10.1146/annurev.genet.35.102401.090231 Bouchenak-Khelladi, 2010, The evolutionary history and biogeography of Mimosoideae (Leguminosae): an emphasis on frican acacias, Mol. Phylogen. Evol., 57, 495, 10.1016/j.ympev.2010.07.019 Bozsoki, 2020, Ligand-recognizing motifs in plant LysM receptors are major determinants of specificity, Science, 369, 663, 10.1126/science.abb3377 Bruneau, 2001, Phylogenetic relationships in the Caesalpinioideae (Leguminosae) as inferred from chloroplast trnL intron sequences, Syst. Bot., 26, 487 Bruneau, 2008, Phylogenetic patterns and diversification in the caesalpinioid legumes, Botany, 86, 697, 10.1139/B08-058 Buendia, 2018, LysM receptor-like kinase and LysM receptor-like protein families: an update on phylogeny and functional characterization, Front. Plant Sci., 9, 1531, 10.3389/fpls.2018.01531 Cannon, 2015, Multiple polyploidy events in the early radiation of nodulating and nonnodulating legumes, Mol. Biol. Evol., 32, 193, 10.1093/molbev/msu296 Cannon, 2006, Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes, Proc. Natl. Acad. Sci. U S A, 103, 14959, 10.1073/pnas.0603228103 Capella-Gutierrez, 2009, trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, 25, 1972, 10.1093/bioinformatics/btp348 Cardoso, 2012, Revisiting the phylogeny of papilionoid legumes: new insights from comprehensively sampled early-branching lineages, Am. J. Bot., 99, 1991, 10.3732/ajb.1200380 Cardoso, 2013, Reconstructing the deep-branching relationships of the papilionoid legumes, S. Afr. J. Bot., 89, 58, 10.1016/j.sajb.2013.05.001 Chappill, 1995, A phylogenetic assessment of tribe Acacieae, 77 Clavijo, 2015, The Casuarina NIN gene is transcriptionally activated throughout Frankia root infection as well as in response to bacterial diffusible signals, New Phytol., 208, 887, 10.1111/nph.13506 Condamine, 2013, Macroevolutionary perspectives to environmental change, Ecol. Lett., 16, 72, 10.1111/ele.12062 Davis, 2014, Plastid phylogenomics and green plant phylogeny: almost full circle but not quite there, BMC Biol., 12, 11, 10.1186/1741-7007-12-11 de la Estrella, 2018, A new phylogeny-based tribal classification of subfamily Detarioideae, an early branching clade of florally diverse tropical arborescent legumes, Sci. Rep., 8, 6884, 10.1038/s41598-018-24687-3 De Mita, 2014, Evolution of a symbiotic receptor through gene duplications in the legume–rhizobium mutualism, New Phytol., 201, 961, 10.1111/nph.12549 de Queiroz, 2015, A multilocus phylogenetic analysis reveals the monophyly of a recircumscribed papilionoid legume tribe Diocleae with well-supported generic relationships, Mol. Phylogen. Evol., 90, 1, 10.1016/j.ympev.2015.04.016 Dos Santos, 2012, Distribution of nitrogen fixation and nitrogenase-like sequences amongst microbial genomes, BMC Genomics, 13, 162, 10.1186/1471-2164-13-162 Doyle, 1977, Angiosperm pollen from the pre-Albian Lower Cretaceous of Equatorial Africa, Bull. Cent. Rech. Explor. Prod. Elf-aquitaine, 1, 451 Doyle, 1994, Phylogeny of the legume family: an approach to understanding the origins of nodulation, Annu. Rev. Ecol. Syst., 25, 325, 10.1146/annurev.es.25.110194.001545 Doyle, 1998, Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria, Trends Plant Sci., 3, 473, 10.1016/S1360-1385(98)01340-5 Doyle, 2011, Phylogenetic perspectives on the origins of nodulation, Mol. Plant Microbe Interact., 24, 1289, 10.1094/MPMI-05-11-0114 Doyle, 2012, Polyploidy in legumes, 147 Doyle, 2016, Chasing unicorns: nodulation origins and the paradox of novelty, Am. J. Bot., 103, 1865, 10.3732/ajb.1600260 Doyle, 2010, Dating the origins of polyploidy events, New Phytol., 186, 73, 10.1111/j.1469-8137.2009.03118.x Du, 2010, agriGO: a GO analysis toolkit for the agricultural community., Nucleic Acids Res, 38, W64, 10.1093/nar/gkq310 Ebersberger, 2009, HaMStR: profile hidden Markov model based search for orthologs in ESTs, BMC Evol. Biol., 9, 157, 10.1186/1471-2148-9-157 Egan, 2010, A comparison of global, gene-specific, soybean (Glycine max), Syst. Biol., 59, 534, 10.1093/sysbio/syq041 Egan, 2019, Advances in legume research in the genomics era, Aust. Syst. Bot., 32, 459, 10.1071/SB19019 Egan, 2016, Parsing polyphyletic Pueraria: delimiting distinct evolutionary lineages through phylogeny, Mol. Phylogen. Evol., 104, 44, 10.1016/j.ympev.2016.08.001 Enright, 2002, An efficient algorithm for large-scale detection of protein families, Nucleic Acids Res, 30, 1575, 10.1093/nar/30.7.1575 Erwin, 2009, Climate as a driver of evolutionary change, Curr. Biol., 19, R575, 10.1016/j.cub.2009.05.047 FitzJohn, 2009, Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies, Syst. Biol., 58, 595, 10.1093/sysbio/syp067 Freeling, 2006, Gene-balanced duplications, like tetraploidy, provide predictable drive to increase morphological complexity, Genome Res., 16, 805, 10.1101/gr.3681406 Fu, 2012, CD-HIT: accelerated for clustering the next-generation sequencing data, Bioinformatics, 28, 3150, 10.1093/bioinformatics/bts565 Garg, 2009, Symbiotic nitrogen fixation in legume nodules: process and signaling: a review, 519 Grabherr, 2011, Full-length transcriptome assembly from RNA-seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Gregg, 2017, Gene-tree reconciliation with MUL-trees to resolve polyploidy events, Syst. Biol., 66, 1007, 10.1093/sysbio/syx044 Griesmann, 2018, Phylogenomics reveals multiple losses of nitrogen-fixing root nodule symbiosis, Science, 361, eaat1743, 10.1126/science.aat1743 Guo, 2020, Phylotranscriptomics in Cucurbitaceae reveal multiple whole-genome duplications and key morphological and molecular innovations, Mol. Plant, 13, 1, 10.1016/j.molp.2020.05.011 Handberg, 1992, Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics, Plant J., 2, 487, 10.1111/j.1365-313X.1992.00487.x Hane, 2017, A comprehensive draft genome sequence for lupin (Lupinus angustifolius), an emerging health food: insights into plant-microbe interactions and legume evolution, Plant Biotechnol. J., 15, 318, 10.1111/pbi.12615 Herendeen, 2003, Phylogenetic relationships in caesalpinioid legumes: a preliminary analysis based on morphological and molecular data, 37 Hu, 2000, Phylogenetic systematics of the tribe Millettieae (Leguminosae) based on chloroplast trnK/matK sequences and its implications for evolutionary patterns in Papilionoideae, Am. J. Bot., 87, 418, 10.2307/2656638 Huang, 2016, Resolution of Brassicaceae phylogeny using nuclear genes uncovers nested radiations and supports convergent morphological evolution, Mol. Biol. Evol., 33, 394, 10.1093/molbev/msv226 Huang, 2016, Multiple polyploidization events across Asteraceae with two nested events in the early history revealed by nuclear phylogenomics, Mol. Biol. Evol., 33, 2820, 10.1093/molbev/msw157 Hughes, 2006, Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes, Proc. Natl. Acad. Sci. U S A, 103, 10334, 10.1073/pnas.0601928103 Jiao, 2012, A genome triplication associated with early diversification of the core eudicots, Genome Biol., 13, R3, 10.1186/gb-2012-13-1-r3 Jiao, 2014, Integrated syntenic and phylogenomic analyses reveal an ancient genome duplication in monocots, Plant Cell, 26, 2792, 10.1105/tpc.114.127597 Jiao, 2011, Ancestral polyploidy in seed plants and angiosperms, Nature, 473, 97, 10.1038/nature09916 Käss, 1996, Molecular evolution of the Leguminosae: phylogeny of the three subfamilies based on rbcL-sequences, Biochem. Syst. Ecol., 24, 365, 10.1016/0305-1978(96)00032-4 Kajita, 2001, rbcL and legume phylogeny, with particular reference to Phaseoleae, Millettieae, and allies, Syst. Bot., 26, 515 Katoh, 2013, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol., 30, 772, 10.1093/molbev/mst010 Knapp, 2005, Relaxed molecular clock provides evidence for long-distance dispersal of Nothofagus (southern beech), PLoS Biol., 3, 38, 10.1371/journal.pbio.0030014 Koenen, 2020, Hybrid capture of 964 nuclear genes resolves evolutionary relationships in the mimosoid legumes and reveals the polytomous origins of a large pantropical radiation, Am J Bot., 107, 1710, 10.1002/ajb2.1568 Koenen, 2020, Large-scale genomic sequence data resolve the deepest divergences in the legume phylogeny and support a near-simultaneous evolutionary origin of all six subfamilies, New Phytol., 225, 1355, 10.1111/nph.16290 Koenen, 2020, The origin of the legumes is a complex paleopolyploid phylogenomic tangle closely associated with the Cretaceous-Paleogene (K-Pg) mass extinction event, Syst. Biol. Konishi, 2013, Arabidopsis NIN-like transcription factors have a central role in nitrate signalling, Nat. Commun., 4, 1617, 10.1038/ncomms2621 Kyalangalilwa, 2013, Phylogenetic position and revised classification of Acacia s.l. (Fabaceae: Mimosoideae) in Africa, including new combinations in Vachellia and Senegalia, Bot. J. Linn. Soc., 172, 500, 10.1111/boj.12047 Larsson, 2014, AliView: a fast and lightweight alignment viewer and editor for large datasets, Bioinformatics, 30, 3276, 10.1093/bioinformatics/btu531 Lavin, 2005, Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary, Syst. Biol., 54, 575, 10.1080/10635150590947131 Leebens-Mack, 2019, One thousand plant transcriptomes and the phylogenomics of green plants, Nature, 574, 679, 10.1038/s41586-019-1693-2 Lewis, 2005 Li, 2015, Large-scale phylogenetic analyses reveal multiple gains of actinorhizal nitrogen-fixing symbioses in angiosperms associated with climate change, Sci. Rep., 5, 14023, 10.1038/srep14023 Li, 2013, Comparative genomics suggests that an ancestral polyploidy event leads to enhanced root nodule symbiosis in the Papilionoideae, Mol. Biol. Evol., 30, 2602, 10.1093/molbev/mst152 Li, 2017, Single-copy genes as molecular markers for phylogenomic studies in seed plants, Genome Biol. Evol., 9, 1130, 10.1093/gbe/evx070 Limpens, 2003, LysM domain receptor kinases regulating rhizobial Nod factor-induced infection, Science, 302, 630, 10.1126/science.1090074 Lohaus, 2016, Of dups and dinos: evolution at the K/Pg boundary, Curr. Opin. Plant Biol., 30, 62, 10.1016/j.pbi.2016.01.006 LPWG, 2013, Towards a new classification system for legumes: progress report from the 6th International Legume Conference, S. Afr. J. Bot., 89, 3, 10.1016/j.sajb.2013.07.022 LPWG, 2017, A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny, Taxon, 66, 44, 10.12705/661.3 Lu, 2018, Evolutionary history of the angiosperm flora of China, Nature, 554, 234, 10.1038/nature25485 Luckow, 2003, A phylogenetic analysis of the Mimosoideae (Leguminosae) based on chloroplast DNA sequence data, 197 Luo, 2012, SOAPdenovo2: an empirically improved memory-efficient short-read de novo assembler, GigaScience, 1, 18, 10.1186/2047-217X-1-18 Maddison Maddison, 2007, Estimating a binary character's effect on speciation and extinction, Syst. Biol., 56, 701, 10.1080/10635150701607033 Mandel, 2019, A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae, Proc. Natl. Acad. Sci. U S A, 116, 14083, 10.1073/pnas.1903871116 Manzanilla, 2012, Phylogeny reconstruction in the Caesalpinieae grade (Leguminosae) based on duplicated copies of the sucrose synthase gene and plastid markers, Mol. Phylogen. Evol., 65, 149, 10.1016/j.ympev.2012.05.035 Mason, 2015, Unreduced gametes: meiotic mishap or evolutionary mechanism?, Trends Genet., 31, 5, 10.1016/j.tig.2014.09.011 Murakami, 2018, Epidermal LysM receptor ensures robust symbiotic signalling in Lotus japonicus, ife, 7, e33506 Nguyen, 2015, IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol Biol Evol, 32, 268, 10.1093/molbev/msu300 Pertea, 2003, TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets, Bioinformatics, 19, 651, 10.1093/bioinformatics/btg034 Prenner, 2008, Towards unlocking the deep nodes of Leguminosae: floral development and morphology of the enigmatic Duparquetia orchidacea (Leguminosae, Caesalpinioideae), Am. J. Bot., 95, 1349, 10.3732/ajb.0800199 Qi, 2018, A well-resolved fern nuclear phylogeny reveals the evolution history of numerous transcription factor families, Mol. Phylogen. Evol., 127, 961, 10.1016/j.ympev.2018.06.043 Ren, 2018, Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms, Mol. Plant, 11, 414, 10.1016/j.molp.2018.01.002 Roy, 2020, Celebrating 20 years of genetic discoveries in legume nodulation and symbiotic nitrogen fixation, Plant Cell, 32, 15, 10.1105/tpc.19.00279 Rutten, 2020, Duplication of symbiotic lysin motif receptors predates the evolution of nitrogen-fixing nodule symbiosis, Plant Physiol., 184, 1004, 10.1104/pp.19.01420 Sanderson, 2002, Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach, Mol. Biol. Evol., 19, 101, 10.1093/oxfordjournals.molbev.a003974 Schmutz, 2010, Genome sequence of the palaeopolyploid soybean, Nature, 463, 178, 10.1038/nature08670 Schmutz, 2014, A reference genome for common bean and genome-wide analysis of dual domestications, Nat. Genet., 46, 707, 10.1038/ng.3008 Shen, 2017, Large-scale phylogenomic analysis resolves a backbone phylogeny in ferns, GigaScience, 7, gix116 Silveira, 2016, Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority, Plant Soil, 403, 129, 10.1007/s11104-015-2637-8 Simão, 2015, BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs., Bioinformatics, 31, 3210, 10.1093/bioinformatics/btv351 Smith, 2012, treePL: divergence time estimation using penalized likelihood for large phylogenies, Bioinformatics, 28, 2689, 10.1093/bioinformatics/bts492 Soltis, 1995, Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms, Proc. Natl. Acad. Sci. U S A, 92, 2647, 10.1073/pnas.92.7.2647 Spehn, 2002, The role of legumes as a component of biodiversity in a cross-European study of grassland biomass nitrogen, Oikos, 98, 205, 10.1034/j.1600-0706.2002.980203.x Sprent, 2009 Springer, 2001, Mitochondrial versus nuclear gene sequences in deep-level mammalian phylogeny reconstruction, Mol. Biol. Evol., 18, 132, 10.1093/oxfordjournals.molbev.a003787 Stai, 2019, Cercis: a non-polyploid genomic relic within the generally polyploid legume family, Front. Plant Sci., 10, 345, 10.3389/fpls.2019.00345 Stamatakis, 2014, RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies, Bioinformatics, 30, 1312, 10.1093/bioinformatics/btu033 Stefanović, 2009, Relationships among Phaseoloid legumes based on sequences from eight chloroplast regions, Syst. Bot., 34, 115, 10.1600/036364409787602221 Suyama, 2006, PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments, Nucleic Acids Res., 34, W609, 10.1093/nar/gkl315 Suzuki, 2013, The evolutionary events necessary for the emergence of symbiotic nitrogen fixation in legumes may involve a loss of nitrate responsiveness of the NIN transcription factor, Plant Signal. Behav., 8, e25975, 10.4161/psb.25975 Thomas, 2017, Gene-tree reconciliation with MUL-trees to resolve polyploidy events, Syst. Biol., 66, 1007, 10.1093/sysbio/syx044 Trenchard, 2008, A review of ploidy in the genus Prosopis (Leguminosae), Bot. J. Linn. Soc., 156, 425, 10.1111/j.1095-8339.2007.00712.x van Velzen, 2019, A resurrected scenario: single gain and massive loss of nitrogen-fixing nodulation, Trends Plant Sci., 24, 49, 10.1016/j.tplants.2018.10.005 van Velzen, 2018, Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses, Proc. Natl. Acad. Sci. U S A, 115, E4700, 10.1073/pnas.1721395115 van Velzen, 2017, Parallel loss of symbiosis genes in relatives of nitrogen-fixing non-legume Parasponia, bioRxiv, 169706 Vandermeer, 1989 Vandermeer, 1990, Agroecology. Intercropping, 481 Vanneste, 2014, Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary, Genome Res., 24, 1334, 10.1101/gr.168997.113 Vatanparast, 2018, Targeting legume loci: a comparison of three methods for target enrichment bait design in Leguminosae phylogenomics, Appl. Plant Sci., 6, e1036, 10.1002/aps3.1036 Veizer, 2000, Evidence for decoupling of atmospheric CO2 and global climate during the Phanerozoic eon, Nature, 408, 698, 10.1038/35047044 Wang, 2010, KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies, Genomics Proteomics Bioinformatics, 8, 77, 10.1016/S1672-0229(10)60008-3 Wang, 2012, MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity, Nucleic Acids Res, 40, 10.1093/nar/gkr1293 Wang, 2017, Hierarchically aligning 10 legume genomes establishes a family-level genomics platform, Plant Physiol., 174, 284, 10.1104/pp.16.01981 Wang, 2018, Plastid genome evolution in the early-diverging legume subfamily Cercidoideae (Fabaceae), Front. Plant Sci., 9, 138, 10.3389/fpls.2018.00138 Wen, 2015, Utility of transcriptome sequencing for phylogenetic inference and character evolution, 1 Werner, 2014, A single evolutionary innovation drives the deep evolution of symbiotic N2-fixation in angiosperms, Nat. Commun., 5, 4087, 10.1038/ncomms5087 Wickett, 2014, Phylotranscriptomic analysis of the origin and early diversification of land plants, Proc. Natl. Acad. Sci. USA, 111, E4859, 10.1073/pnas.1323926111 Wojciechowski, 2003, Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perspective, 5 Wojciechowski, 2004, A phylogeny of legumes (Leguminosae) based on analysis of the plastid matK gene resolves many well-supported subclades within the family, Am. J. Bot., 91, 1846, 10.3732/ajb.91.11.1846 Xiang, 2017, Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication, Mol. Biol. Evol., 34, 262 Yang, 2018, Improved transcriptome sampling pinpoints 26 ancient and more recent polyploidy events in Caryophyllales, including two allopolyploidy events, New Phytol., 217, 855, 10.1111/nph.14812 Yang, 2006 Young, 2011, The Medicago genome provides insight into the evolution of rhizobial symbioses, Nature, 480, 520, 10.1038/nature10625 Zachos, 2008, An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics, Nature, 451, 279, 10.1038/nature06588 Zahran, 1999, Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate, Microbiol. Mol. Biol. Rev., 63, 968, 10.1128/MMBR.63.4.968-989.1999 Zeng, 2017, Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets, New Phytol., 214, 1338, 10.1111/nph.14503 Zeng, 2014, Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times, Nat. Commun., 5, 4956, 10.1038/ncomms5956 Zhang, 2018, ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees, BMC Bioinformatics, 19, 153, 10.1186/s12859-018-2129-y Zhang, 2015, Genome-wide association study for flowering time, maturity dates and plant height in early maturing soybean (Glycine max) germplasm, BMC Genomics, 16, 217, 10.1186/s12864-015-1441-4 Zhang, 2009, Phylogeny of Caragana (Fabaceae) based on DNA sequence data from rbcL, trnS–trnG, and ITS, Mol. Phylogen. Evol., 50, 547, 10.1016/j.ympev.2008.12.001 Zhang, 2012, Highly conserved low-copy nuclear genes as effective markers for phylogenetic analyses in angiosperms, New Phytol., 195, 923, 10.1111/j.1469-8137.2012.04212.x Zhang, 2020, The water lily genome and the early evolution of flowering plants, Nature, 577, 79, 10.1038/s41586-019-1852-5 Zhang, 2020, Exploration of plastid phylogenomic conflict yields new insights into the deep relationships of Leguminosae, Syst. Biol., 69, 613, 10.1093/sysbio/syaa013 Zhang, 2020, Asterid phylogenomics/phylotranscriptomics uncover morphological evolutionary histories and support phylogenetic placement for numerous whole-genome duplications, Mol. Biol. Evol., 69 Zhao, 2016, Phylogenomic analyses of large-scale nuclear genes provide new insights into the evolutionary relationships within the rosids, Mol. Phylogen. Evol., 105, 166, 10.1016/j.ympev.2016.06.007 Zhuang, 2019, The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication, Nat. Genet., 51, 865, 10.1038/s41588-019-0402-2 Zimmerman, 2017, Floral evolution and phylogeny of the Dialioideae, a diverse subfamily of tropical legumes, Am. J. Bot., 104, 1019, 10.3732/ajb.1600436