Phylogenomics insights into gene evolution, rapid species diversification, and morphological innovation of the apple tribe (Maleae, Rosaceae)
Lin Zhang
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
These authors contributed equally to this work.
Search for more papers by this authorDiego F. Morales-Briones
Princess Therese von Bayern chair of Systematics, Biodiversity and Evolution of Plants, Ludwig-Maximilians-Universität München, Menzinger Str. 67, Munich, 80638 Germany
These authors contributed equally to this work.
Search for more papers by this authorYujie Li
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
Search for more papers by this authorGuojin Zhang
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Search for more papers by this authorTaikui Zhang
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, 200433 China
Search for more papers by this authorChien-Hsun Huang
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, 200433 China
Search for more papers by this authorPeng Guo
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Life Science, Henan Agricultural University, Zhengzhou, 450002 China
Search for more papers by this authorKaiming Zhang
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
Search for more papers by this authorCorresponding Author
Yihan Wang
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Life Science, Henan Agricultural University, Zhengzhou, 450002 China
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorCorresponding Author
Hongwei Wang
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Plant Protection, Henan Agricultural University, Zhengzhou, 450002 China
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorCorresponding Author
Fu-De Shang
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Life Science, Henan Agricultural University, Zhengzhou, 450002 China
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorCorresponding Author
Hong Ma
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorLin Zhang
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
These authors contributed equally to this work.
Search for more papers by this authorDiego F. Morales-Briones
Princess Therese von Bayern chair of Systematics, Biodiversity and Evolution of Plants, Ludwig-Maximilians-Universität München, Menzinger Str. 67, Munich, 80638 Germany
These authors contributed equally to this work.
Search for more papers by this authorYujie Li
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
Search for more papers by this authorGuojin Zhang
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Search for more papers by this authorTaikui Zhang
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, 200433 China
Search for more papers by this authorChien-Hsun Huang
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, School of Life Sciences, Fudan University, Shanghai, 200433 China
Search for more papers by this authorPeng Guo
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Life Science, Henan Agricultural University, Zhengzhou, 450002 China
Search for more papers by this authorKaiming Zhang
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
Search for more papers by this authorCorresponding Author
Yihan Wang
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Life Science, Henan Agricultural University, Zhengzhou, 450002 China
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorCorresponding Author
Hongwei Wang
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Plant Protection, Henan Agricultural University, Zhengzhou, 450002 China
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorCorresponding Author
Fu-De Shang
College of Landscape Architecture and Art, Henan Agricultural University, Zhengzhou, 450002 China
Henan Engineering Research Center for Osmanthus Germplasm Innovation and Resource Utilization, Henan Agricultural University, Zhengzhou, 450002 China
College of Life Science, Henan Agricultural University, Zhengzhou, 450002 China
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorCorresponding Author
Hong Ma
Department of Biology, The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802 USA
Authors for correspondence:
Hong Ma
Email:[email protected]
Fu-De Shang
Email:[email protected]
Hongwei Wang
Email:[email protected]
Yihan Wang
Email:[email protected]
Search for more papers by this authorSummary
- Maleae is one of the most widespread tribes of Rosaceae and includes several important fruit crops and ornamental plants.
- We used nuclear genes from 62 transcriptomes/genomes, including 26 newly generated transcriptomes, to reconstruct a well-supported phylogeny and study the evolution of fruit and leaf morphology and the possible effect of whole genome duplication (WGD).
- Our phylogeny recovered 11 well-supported clades and supported the monophyly of most genera (except Malus, Sorbus, and Pourthiaea) with at least two sampled species. A WGD was located to the most recent common ancestor (MRCA) of Maleae and dated to c. 54 million years ago (Ma) near the Early Eocene Climatic Optimum, supporting Gillenieae (x = 9) being a parental lineage of Maleae (x = 17) and including duplicate regulatory genes related to the origin of the fleshy pome fruit. Whole genome duplication-derived paralogs that are retained in specific lineages but lost in others are predicted to function in development, metabolism, and other processes. An upshift of diversification and innovations of fruit and leaf morphologies occurred at the MRCA of the Malinae subtribe, coinciding with the Eocene–Oligocene transition (c. 34 Ma), following a lag from the time of the WGD event.
- Our results provide new insights into the Maleae phylogeny, its rapid diversification, and morphological and molecular evolution.
Open Research
Data availability
The RNA-seq raw datasets were uploaded to NCBI SRA database with accession number of PRJNA917232. All assembled sequence data reported in this paper are available from the figshare website (doi: 10.6084/m9.figshare.23584401).
Supporting Information
| Filename | Description |
|---|---|
| nph19175-sup-0001-FigsS1-S18.pdfPDF document, 4 MB | Fig. S1 A comparison of Maleae phylogenies at the genus level from previous reports and this study. Fig. S2 The workflow and species tree inference used in this study. Fig. S3 A phylogeny inferred from 10 564 gene families by Astral-Pro. Fig. S4 A phylogeny inferred from 2114 orthologs by Astral. Fig. S5 A phylogeny from maximum likelihood analysis using a dataset of concatenated 2114 orthologs. Fig. S6 A phylogeny from maximum likelihood analysis using a dataset of concatenated 67 plastid coding genes. Fig. S7 A summary of GD bursts in Maleae from a data set of 62 species. Fig. S8 Number of GDs mapped at the most recent common ancestor of subtribe in different type shared by paralogs in each species from data sets of 20 species. Fig. S9 A summary of the origin of Maleae. Fig. S10 A detailed molecular phylogeny of the AG homologs in MADS-box gene family. Fig. S11 A detailed molecular phylogeny of the STK homologs in MADS-box gene family. Fig. S12 A detailed molecular phylogeny of the FUL homologs in MADS-box gene family. Fig. S13 A detailed molecular phylogeny of the AP1 homologs in MADS-box gene family. Fig. S14 A detailed molecular phylogeny of the SVP homologs in MADS-box gene family. Fig. S15 A detailed molecular phylogeny of the SHP homologs in MADS-box gene family. Fig. S16 A detailed molecular phylogeny of the SOC1 homologs in MADS-box gene family. Fig. S17 Divergence times of Maleae. Fig. S18 Ancestral character state reconstruction of petal color. |
| nph19175-sup-0002-TablesS1-S8.xlsxExcel 2007 spreadsheet , 120.6 KB | Table S1 Summary of Maleae samples included in this study. Table S2 Information on all species included in this study. Table S3 Species information was to construct plastid phylogeny from NCBI in this study. Table S4 Information on 20 species included in this study. Table S5 Fossil calibrations used for divergence time estimation. Table S6 Characters information used in ancestral state reconstruction. Table S7 List of ancestral genes retained in pair in the species and in single copy in other species. Table S8 List of GO terms enriched in five species between ancestral genes from WGD. Please note: Wiley is not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
References
- Bardou P, Mariette J, Escudie F, Djemiel C, Klopp C. 2014. jvenn: an interactive Venn diagram viewer. BMC Bioinformatics 15: 293.
- Beaulieu JM, Donoghue MJ. 2013. Fruit evolution and diversification in campanulid angiosperms. Evolution 67: 3132–3144.
- Cai L, Xi Z, Lemmon EM, Lemmon AR, Mast A, Buddenhagen CE, Liu L, Davis CC. 2021. The perfect storm: gene tree estimation error, incomplete lineage sorting, and ancient gene flow explain the most recalcitrant ancient Angiosperm clade, Malpighiales. Systematic Biology 70: 491–507.
- Campbell CS, Evans RC, Morgan DR, Dickinson TA, Arsenault MP. 2007. Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): limited resolution of a complex evolutionary history. Plant Systematics and Evolution 266: 119–145.
- Cazetta E, Schaefer HM, Galetti M. 2009. Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evolutionary Ecology 23: 233–244.
- Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. 2020. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant 13: 1194–1202.
- Chen D, Zhang T, Chen Y, Ma H, Qi J. 2022. Tree2GD: a phylogenomic method to detect large-scale gene duplication events. Bioinformatics 38: 5317–5321.
- Chen S, Zhou Y, Chen Y, Gu J. 2018. Fastp: an ultra-fast all-in-one Fastq preprocessor. Bioinformatics 34: i884–i890.
- Daccord N, Celton JM, Linsmith G, Becker C, Choisne N, Schijlen E, van de Geest H, Bianco L, Micheletti D, Velasco R et al. 2017. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nature Genetics 49: 1099–1106.
- Davis CC, Xi Z, Mathews S. 2014. Plastid phylogenomics and green plant phylogeny: almost full circle but not quite there. BMC Biology 12: 11.
- van Dongen S, Abreu-Goodger C. 2012. Using Mcl to extract clusters from networks. Methods in Molecular Biology 804: 281–295.
- Emms DM, Kelly S. 2015. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biology 16: 157.
- Eriksson O. 2008. Evolution of seed size and biotic seed dispersal in Angiosperms: paleoecological and neoecological evidence. International Journal of Plant Sciences 169: 863–870.
- Evans RC, Campbell CS. 2002. The origin of the apple subfamily (Maloideae; Rosaceae) is clarified by DNA sequence data from duplicated GBSSI genes. American Journal of Botany 89: 1478–1484.
- Fawcett JA, Maere S, Van de Peer Y. 2009. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proceedings of the National Academy of Sciences, USA 106: 5737–5742.
- Fu L, Niu B, Zhu Z, Wu S, Li W. 2012. Cd-hit: accelerated for clustering the next-generation sequencing data. Bioinformatics 28: 3150–3152.
- Garcia-Hernandez M, Berardini TZ, Chen G, Crist D, Doyle A, Huala E, Knee E, Lambrecht M, Miller N, Mueller LA et al. 2002. Tair: a resource for integrated Arabidopsis data. Functional & Integrative Genomics 2: 239–253.
- Ge J, Berg B, Xie Z. 2019. Climatic seasonality is linked to the occurrence of the mixed evergreen and deciduous broad-leaved forests in China. Ecosphere 10: e02862.
- Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q et al. 2011. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology 29: 644–652.
- Gratani L. 2014. Plant phenotypic plasticity in response to environmental factors. Advances in Botany 2014: 1–17.
10.1155/2014/208747 Google Scholar
- Hodel RGJ, Zimmer EA, Liu BB, Wen J. 2021. Synthesis of nuclear and chloroplast data combined with network analyses supports the polyploid origin of the apple tribe and the hybrid origin of the Maleae-Gillenieae clade. Frontiers in Plant Science 12: 820997.
- Janssen BJ, Thodey K, Schaffer RJ, Alba R, Balakrishnan L, Bishop R, Bowen JH, Crowhurst RN, Gleave AP, Ledger S et al. 2008. Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biology 8: 16.
- Jaramillo C, Ochoa D, Contreras L, Pagani M, Carvajal-Ortiz H, Pratt LM, Krishnan S, Cardona A, Romero M, Quiroz L et al. 2010. Effects of rapid global warming at the Paleocene-Eocene boundary on neotropical vegetation. Science 330: 957–961.
- Johnson JS, Cantrell RS, Cosner C, Hartig F, Hastings A, Rogers HS, Schupp EW, Shea K, Teller BJ, Yu X et al. 2019. Rapid changes in seed dispersal traits may modify plant responses to global change. AoB Plants 11: plz020.
- Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589.
- Kassahn KS, Dang VT, Wilkins SJ, Perkins AC, Ragan MA. 2009. Evolution of gene function and regulatory control after whole-genome duplication: comparative analyses in vertebrates. Genome Research 19: 1404–1418.
- Katoh K, Standley DM. 2013. Mafft multiple sequence alignment software v.7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.
- Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C et al. 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.
- Khoo HE, Azlan A, Tang ST, Lim SM. 2017. Anthocyanidins and anthocyanins: colored pigments as food, pharmaceutical ingredients, and the potential health benefits. Food & Nutrition Research 61: 1361779.
- Koenen EJM, Kidner C, de Souza ER, Simon MF, Iganci JR, Nicholls JA, Brown GK, de Queiroz LP, Luckow M, Lewis GP et al. 2020. Hybrid capture of 964 nuclear genes resolves evolutionary relationships in the mimosoid legumes and reveals the polytomous origins of a large pantropical radiation. American Journal of Botany 107: 1710–1735.
- Landis JB, Soltis DE, Li Z, Marx HE, Barker MS, Tank DC, Soltis PS. 2018. Impact of whole-genome duplication events on diversification rates in angiosperms. American Journal of Botany 105: 348–363.
- Lanfear R, Calcott B, Ho SY, Guindon S. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29: 1695–1701.
- Liu BB, Campbell CS, Hong DY, Wen J. 2020. Phylogenetic relationships and chloroplast capture in the Amelanchier-Malacomeles-Peraphyllum clade (Maleae, Rosaceae): evidence from chloroplast genome and nuclear ribosomal DNA data using genome skimming. Molecular Phylogenetics and Evolution 147: 106784.
- Liu BB, Hong DY, Zhou SL, Xu C, Dong WP, Johnson G, Wen J. 2019. Phylogenomic analyses of the Photinia complex support the recognition of a new genus Phippsiomeles and the resurrection of a redefined Stranvaesia in Maleae (Rosaceae). Journal of Systematics and Evolution 57: 678–694.
- Liu BB, Ren C, Kwak M, Hodel RGJ, Xu C, He J, Zhou WB, Huang CH, Ma H, Qian GZ et al. 2022. Phylogenomic conflict analyses in the apple genus Malus s.l. reveal widespread hybridization and allopolyploidy driving diversification, with insights into the complex biogeographic history in the Northern Hemisphere. Journal of Integrative Plant Biology 64: 1020–1043.
- Lo EY, Donoghue MJ. 2012. Expanded phylogenetic and dating analyses of the apples and their relatives (Pyreae, Rosaceae). Molecular Phylogenetics and Evolution 63: 230–243.
- Lu LM, Mao LF, Yang T, Ye JF, Liu B, Li HL, Sun M, Miller JT, Mathews S, Hu HH et al. 2018. Evolutionary history of the angiosperm flora of China. Nature 554: 234–238.
- Mai U, Mirarab S. 2018. TreeShrink: fast and accurate detection of outlier long branches in collections of phylogenetic trees. BMC Genomics 19: 272.
- Malhado ACM, Whittaker RJ, Malhi Y, Ladle RJ, Ter Steege H, Phillips O, Aragão LEOC, Baker TR, Arroyo L, Almeida S et al. 2010. Are compound leaves an adaptation to seasonal drought or to rapid growth? Evidence from the Amazon rain forest. Global Ecology and Biogeography 19: 852–862.
- Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R. 2020. IQ-Tree 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37: 1530–1534.
- Mirarab S, Nguyen N, Guo S, Wang LS, Kim J, Warnow T. 2015. Pasta: ultra-large multiple sequence alignment for nucleotide and amino-acid sequences. Journal of Computational Biology 22: 377–386.
- Morales-Briones DF, Kadereit G, Tefarikis DT, Moore MJ, Smith SA, Brockington SF, Timoneda A, Yim WC, Cushman JC, Yang Y. 2021. Disentangling sources of gene tree discordance in phylogenomic data sets: testing ancient hybridizations in Amaranthaceae s.l. Systematic Biology 70: 219–235.
- Mulch A, Chamberlain CP, Cosca MA, Teyssier C, Methner K, Hren MT, Graham SA. 2015. Rapid change in high-elevation precipitation patterns of western North America during the Middle Eocene Climatic Optimum (MECO). American Journal of Science 315: 317–336.
- Niederhauser EC, Matlack GR. 2015. All frugivores are not equal: exploitation competition determines seed survival and germination in a fleshy-fruited forest herb. Plant Ecology 216: 1203–1211.
- Pagani M, Pedentchouk N, Huber M, Sluijs A, Schouten S, Brinkhuis H, Damste JS, Dickens GR, Expedition S. 2006. Arctic hydrology during global warming at the Palaeocene/Eocene thermal maximum. Nature 442: 671–675.
- Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B et al. 2003. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15: 1538–1551.
- Parks MB, Wickett NJ, Alverson AJ. 2018. Signal, uncertainty, and conflict in phylogenomic data for a diverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta). Molecular Biology and Evolution 35: 80–93.
- Phipps JB, Robertson KR, Rohrer JR. 1991. Origins and evolution of subfam. Maloideae (Rosaceae). Systematic Botany 16: 303–332.
- Pohl N, Sison-Mangus MP, Yee EN, Liswi SW, Briscoe AD. 2009. Impact of duplicate gene copies on phylogenetic analysis and divergence time estimates in butterflies. BMC Evolutionary Biology 9: 99.
- Potter D, Eriksson T, Evans R. 2007. Phylogeny and classification of Rosaceae. Plant Systematics and Evolution 266: 5–43.
- Rabosky DL, Grundler M, Anderson C, Title P, Shi JJ, Brown JW, Huang H, Larson JG, Kembel S. 2014. bammtools: an R package for the analysis of evolutionary dynamics on phylogenetic trees. Methods in Ecology and Evolution 5: 701–707.
- Rabosky DL, Santini F, Eastman J, Smith SA, Sidlauskas B, Chang J, Alfaro ME. 2013. Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications 4: 1958.
- Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J. 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in Angiosperms. Molecular Plant 11: 414–428.
- Robertson KR, Phipps JB, Rohrer JR, Smith PG. 1991. A synopsis of genera in Maloideae (Rosaceae). Systematic Botany 16: 376–394.
- Sax K. 1931. The origin and relationships of the Pomoideae. Journal of the Arnold Arboretum 12: 3–22.
10.5962/p.185222 Google Scholar
- Sax K. 1933. The origin of the Pomoideae. Proceedings of the American Society of Horticultural Science 30: 147–150.
- Schmerler SB, Clement WL, Beaulieu JM, Chatelet DS, Sack L, Donoghue MJ, Edwards EJ. 2012. Evolution of leaf form correlates with tropical-temperate transitions in Viburnum (Adoxaceae). Proceedings of the Biological Sciences 279: 3905–3913.
- Schranz ME, Mohammadin S, Edger PP. 2012. Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Current Opinion in Plant Biology 15: 147–153.
- Sinnott-Armstrong MA, Lee C, Clement WL, Donoghue MJ. 2020. Fruit syndromes in Viburnum: correlated evolution of color, nutritional content, and morphology in bird-dispersed fleshy fruits. BMC Evolutionary Biology 20: 7.
- Smith SA, Dunn CW. 2008. Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics 24: 715–716.
- Smith-Unna R, Boursnell C, Patro R, Hibberd JM, Kelly S. 2016. TransRate: reference-free quality assessment of de novo transcriptome assemblies. Genome Research 26: 1134–1144.
- Song L, Florea L. 2015. Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads. GigaScience 4: 48.
- Stamatakis A. 2014. RAxML v.8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
- Su W, Jing Y, Lin S, Yue Z, Yang X, Xu J, Wu J, Zhang Z, Xia R, Zhu J et al. 2021. Polyploidy underlies co-option and diversification of biosynthetic triterpene pathways in the apple tribe. Proceedings of the National Academy of Sciences, USA 108: e2101767118.
10.1073/pnas.2101767118 Google Scholar
- Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE, Hinchliff CE, Brown JW, Sessa EB, Harmon LJ. 2015. Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytologist 207: 454–467.
- Theissen G, Melzer R, Rumpler F. 2016. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143: 3259–3271.
- Valenta K, Burke RJ, Styler SA, Jackson DA, Melin AD, Lehman SM. 2013. Colour and odour drive fruit selection and seed dispersal by mouse lemurs. Scientific Reports 3: 2424.
- Vanneste K, Baele G, Maere S, Van de Peer Y. 2014. Analysis of 41 plant genomes supports a wave of successful genome duplications in association with the Cretaceous-Paleogene boundary. Genome Research 24: 1334–1347.
- Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D et al. 2010. The genome of the domesticated apple (Malus x domestica Borkh.). Nature Genetics 42: 833–839.
- Walden N, German DA, Wolf EM, Kiefer M, Rigault P, Huang XC, Kiefer C, Schmickl R, Franzke A, Neuffer B et al. 2020. Nested whole-genome duplications coincide with diversification and high morphological disparity in Brassicaceae. Nature Communications 11: 3795.
- Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H et al. 2012. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research 40: e49.
- Wickett NJ, Mirarab S, Nguyen N, Warnow T, Carpenter E, Matasci N, Ayyampalayam S, Barker MS, Burleigh JG, Gitzendanner MA et al. 2014. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proceedings of the National Academy of Sciences, USA 111: e4859–e4868.
- Wilf P, Labandeira CC, Kress WJ, Staines CL, Windsor DM, Allen AL, Johnson KR. 2000. Timing the radiations of leaf beetles: hispines on gingers from latest cretaceous to recent. Science 289: 291–294.
- Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H et al. 2013. The genome of the pear (Pyrus bretschneideri Rehd.). Genome Research 23: 396–408.
- Xiang Y, Huang CH, Hu Y, Wen J, Li S, Yi T, Chen H, Xiang J, Ma H. 2017. Evolution of Rosaceae fruit types based on nuclear phylogeny in the context of geological times and genome duplication. Molecular Biology and Evolution 34: 262–281.
- Yang Y, Smith SA. 2014. Orthology inference in nonmodel organisms using transcriptomes and low-coverage genomes: improving accuracy and matrix occupancy for phylogenomics. Molecular Biology and Evolution 31: 3081–3092.
- Yang Z. 2007. Paml 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586–1591.
- Yu G, Wang LG, Han Y, He QY. 2012. clusterprofiler: an R package for comparing biological themes among gene clusters. Omics 16: 284–287.
- Zeng L, Zhang N, Zhang Q, Endress PK, Huang J, Ma H. 2017. Resolution of deep eudicot phylogeny and their temporal diversification using nuclear genes from transcriptomic and genomic datasets. New Phytologist 214: 1338–1354.
- Zeng L, Zhang Q, Sun R, Kong H, Zhang N, Ma H. 2014. Resolution of deep angiosperm phylogeny using conserved nuclear genes and estimates of early divergence times. Nature Communications 5: 4956.
- Zhang C, Rabiee M, Sayyari E, Mirarab S. 2018. Astral-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics 19: 153.
- Zhang C, Scornavacca C, Molloy EK, Mirarab S. 2020. Astral-Pro: quartet-based species-tree inference despite paralogy. Molecular Biology and Evolution 37: 3292–3307.
- Zhang N, Zeng L, Shan H, Ma H. 2012. Highly conserved low-copy nuclear genes as effective markers for phylogenetic analyses in angiosperms. New Phytologist 195: 923–937.
- Zhang SD, Jin JJ, Chen SY, Chase MW, Soltis DE, Li HT, Yang JB, Li DZ, Yi TS. 2017. Diversification of Rosaceae since the Late Cretaceous based on plastid phylogenomics. New Phytologist 214: 1355–1367.
- Zhang T, Qiao Q, Du X, Zhang X, Hou Y, Wei X, Sun C, Zhang R, Yun Q, Crabbe MJC et al. 2022. Cultivated hawthorn (Crataegus pinnatifida var. major) genome sheds light on the evolution of Maleae (apple tribe). Journal of Integrative Plant Biology 64: 1487–1501.
- Zhao D, Zhang Y, Lu Y, Fan L, Zhang Z, Zheng J, Chai M. 2022. Genome sequence and transcriptome of Sorbus pohuashanensis provide insights into population evolution and leaf sunburn response. Journal of Genetics and Genomics 49: 547–558.
Citing Literature
