Biogeographic and metabolic studies support a glacial radiation hypothesis during Chrysanthemum evolution

Xi Chen , Haibin Wang , Jiafu Jiang , Yifan Jiang , Wanbo Zhang , Fadi Chen

Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) : uhac153

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Horticulture Research ›› 2022, Vol. 9 ›› Issue (1) :uhac153 DOI: 10.1093/hr/uhac153
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Biogeographic and metabolic studies support a glacial radiation hypothesis during Chrysanthemum evolution
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Abstract

Chrysanthemum (Chrysanthemum morifolium Ramat.) is an economically important plant species growing worldwide. However, its origin, especially as revealed by biogeographic and metabolomics research, remains unclear. To understand the geographic distribution of species diversity and metabolomics in three genera (Chrysanthemum, Ajania, and Phaeostigma), geographic information systems and gas chromatography–mass spectrometry were used in 19, 15, and 4 species respectively. China and Japan were two potential panbiogeographic nodes and diverse hotspots of Chrysanthemum, with species richness ratios of 58.97 and 33.33%. We studied different species from two hotspots which in similar geographical environments had closer chemotaxonomic relationships under the same cultivation conditions based on a cluster of 30 secondary metabolites. The average distribution altitude (ADA) differed significantly among Chrysanthemum, Ajania, and Phaeostigma in which it was 1227.49, 2400.12, and 3760.53 m.a.s.l. respectively, and the presence/absence of ray florets (RF) was significantly correlated with ADA (−0.62). Mountain landform was an important contributor to global Chrysanthemum diversity, playing a key role in the divergence and distribution pattern of Chrysanthemum and its allies. The Hengduan Mountains–Qinling Mountains (HDQ) in China was a potential secondary radiation and evolution center of Chrysanthemum and its related genera in the world. During the Quaternary glacial–interglacial cycles, this region became their refuge, and they radiated and evolved from this center.

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Xi Chen, Haibin Wang, Jiafu Jiang, Yifan Jiang, Wanbo Zhang, Fadi Chen. Biogeographic and metabolic studies support a glacial radiation hypothesis during Chrysanthemum evolution. Horticulture Research, 2022, 9 (1) : uhac153 DOI:10.1093/hr/uhac153

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References

[1]

Chen JY . The Origin of Garden Chrysanthemum . Hefei: Anhui Science and Technology Press; 2012.

[2]

Su J, Jiang J, Zhang F et al. Current achievements and future prospects in the genetic breeding of chrysanthemum: a review. Hortic Res. 2019; 6: 109.

[3]

Hirakawa H, Sumitomo K, Hisamatsu T et al. De novo whole-genome assembly in Chrysanthemum seticuspe, a model species of Chrysanthemums, and its application to genetic and gene discovery analysis . DNA Res. 2019; 26: 195-203.

[4]

Ma YP, Zhao L, Zhang WJ et al. Origins of cultivars of Chrysanthemum-evidence from the chloroplast genome and nuclear LFY gene . Acta Phytotaxon Sin. 2020; 58: 925-44.

[5]

Liu PL, Wan Q, Guo YP et al. Phylogeny of the genus Chrysanthemum L.: evidence from single-copy nuclear gene and chloroplast DNA sequences. PLoS One. 2012; 7: e48970.

[6]

Põlme S, Bahram M, Kõljalg U et al. Global biogeography of Alnus-associated Frankia actinobacteria . New Phytol. 2014; 204: 979-88.

[7]

Janssens SB, Vandelook F, de Langhe E et al. Evolutionary dynamics and biogeography of Musaceae reveal a correlation between the diversification of the banana family and the geological and climatic history of Southeast Asia. New Phytol. 2016; 210: 1453-65.

[8]

Pérez-Escobar OA, Chomicki G, Condamine FL et al. Recent origin and rapid speciation of Neotropical orchids in the world’s richest plant biodiversity hotspot. New Phytol. 2017; 215: 891-905.

[9]

Shen CZ, Zhang CJ, Chen J et al. Clarifying recent adaptive diversification of the Chrysanthemum-group on the basis of an updated multilocus phylogeny of subtribe Artemisiinae (Asteraceae: Anthemideae) . Front Plant Sci. 2021; 12: 648026.

[10]

Li J, Wan Q, Guo YP et al. Should I stay or should I go: biogeographic and evolutionary history of a polyploid complex (Chrysanthemum indicum complex) in response to Pleistocene climate change in China . New Phytol. 2014; 201: 1031-44.

[11]

Sanz M, Vilatersana R, Hidalgo O et al. Molecular phylogeny and evolution of floral characters of Artemisia and allies (Anthemideae, Asteraceae): evidence from nrDNA ETS and ITS sequences. Taxon. 2008; 57: 1-13.

[12]

Zhao HB, Chen FD, Chen SM et al. Molecular phylogeny of Chrysanthemum, Ajania and ITS allies (Anthemideae, Asteraceae) as inferred from nuclear ribosomal ITS and chloroplast trnL-F IGS sequences . Plant Syst Evol. 2010; 284: 153-69.

[13]

Huang Y, An YM, Meng SY et al. Taxonomic status and phylogenetic position of Phaeostigma in the subtribe Artemisiinae (Asteraceae) . J Syst Evol. 2017; 55: 426-36.

[14]

Sandel B, Weigelt P, Kreft H et al. Current climate, isolation and history drive global patterns of tree phylogenetic endemism. Glob Ecol Biogeogr. 2020; 29: 4-15.

[15]

Ye Z, Yuan JJ, Zhen Y et al. Local environmental selection and lineage admixture act as significant mechanisms in the adaptation of the widespread east Asian pond skater Gerris latiabdominis to heterogeneous landscapes. J Biogeogr. 2020; 47: 1154-65.

[16]

Moore BD, Andrew RL, Kulheim C et al. Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytol. 2013; 201: 733-50.

[17]

Agrawal AA, Petschenka G, Bingham RA et al. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol. 2012; 194: 28-45.

[18]

Pichersky E, Lewinsohn E . Convergent evolution in plant specialized metabolism. Annu Rev Plant Biol. 2011; 62: 549-66.

[19]

Leong BJ, Lybrand DB, Lou YR et al. Evolution of metabolic novelty: a trichome-expressed invertase creates specialized metabolic diversity in wild tomato. Sci Adv. 2019; 5: eaaw3754.

[20]

Martucci MEP, Loeuille B, Pirani JR et al. Comprehensive untargeted metabolomics of Lychnnophorinae subtribe (Asteraceae: Vernonieae) in a phylogenetic context. PLoS One. 2018; 13: e0190104.

[21]

Gallon ME, Monge M, Casoti R et al. Metabolomic analysis applied to chemosystematics and evolution of megadiverse Brazilian Vernonieae (Asteraceae). Phytochemistry. 2018; 150: 93-105.

[22]

Uehara A, Nakata M, Uchida A et al. Chemotaxonomic consideration of flavonoids from the leaves of Chrysanthemum arcticum subsp. arcticum and yezoense, and related species . Biochem Syst Ecol. 2017; 73: 11-5.

[23]

Yang L, Nuerbiye A, Cheng P et al. Analysis of floral volatile components and antioxidant activity of different varieties of Chrysanthemum morifolium . Molecules. 2018; 22: 1790.

[24]

Zhu Y, Zhang LX, Zhao Y et al. Unusual sesquiterpene lactones with a new carbon skeleton and new acetylenes from Ajania przewalskii . Food Chem. 2010; 118: 228-38.

[25]

Usami A, Nakahashi H, Marumoto S et al. Aroma evaluation of Setonojigiku (Chrysanthemum japonense var. debile) by hydrodistillation and solvent-assisted flavour evaporation. Phytochem Anal. 2014; 25: 561-6.

[26]

Liang JY, Guo SS, You CX et al. Chemical constituents and insecticidal activities of Ajania fruticulosa essential oil. Chem Biodivers. 2016; 13: 1053-7.

[27]

Liang JY, Xu J, Shao YZ et al. Chemical constituents from the aerial sections of Ajania potaninii . Biochem Syst Ecol. 2019; 84: 64-6.

[28]

Ryu J, Nam B, Kim BR et al. Comparative analysis of phytochemical composition of gamma-irradiated mutant cultivars of Chrysanthemum morifolium . Molecules. 2019; 24: 3003.

[29]

Shih C, Fu GX . Flora of China, Vol. 76, Division 1 . Beijing: The Science Publishing Company; 1983: In Chinese.

[30]

Academiae Scientiarum URSS . Flora URSS, Vol. XXVI. Leningrad: Mocqua. 1961; 364-411 In Russian.

[31]

Tutin TG, Heywood VH, Burges NA et al. Flora Europaea, Vol. 4. Cambridge: Cambridge University Press, 1976, 168-9.

[32]

Ohwi J . Flora of Japan . Shibundo, Tokyo, 1956, 1182-8. [In Japanese.]

[33]

Poljakov PP . Duo genere novae fam. Compositae. Not Syst Herb Inst Bot Akad Sci URSS. 1955; 17: 418-31.

[34]

Nakata M, Tanaka R, Taniguchi K et al. Species of wild chrysanthemums in Japan: cytological and cytogenetical view on its entity. Acta Phytotaxon Geobot. 1987; 38: 241-59 [In Japanese].

[35]

Kitamura S. Report on the distribution of the wild chrysanthemums of Japan. Acta Phytotaxon Geobot. 1967; 22: 109-37 [In Japanese].

[36]

Sonboli A, Olanj N, Mozaffarian V et al. Ajania semnanensis sp. nov. (Asteraceae-Anthemideae), from Northeast Iran: insights from karyological and micromorphological data . Nord J Bot. 2013; 31: 590-4.

[37]

Zhao LQ, Yang J, Niu JM et al. Chrysanthemum zhuozishanense (Compositae), a new species in section Chrysanthemum from Inner Mongolia, China . Novon (St Louis). 2014; 23: 255-7.

[38]

Chen JT, Zhong J, Shi XJ et al. Chrysanthemum yantaiense, a rare new species of Asteraceae from China . Phytotaxa. 2018; 374: 92-6.

[39]

Meng S, Wen L, Shen C . Chrysanthemum bizarre, a new species of chrysanthemum from Hunan . China Phytotaxa. 2020; 442: 215-24.

[40]

Moreira-Muñoz A, Muñoz-Schick M . Classification, diversity, and distribution of Chilean Asteraceae: implications for biogeography and conservation. Divers Distrib. 2007; 13: 818-28.

[41]

Huang J, Chen B, Liu C et al. Identifying hotspots of endemic woody seed plant diversity in China. Divers Distrib. 2012; 18: 673-88.

[42]

Jardine EC, Thomas GH, Forrestel EJ et al. The global distribution of grass functional traits within grassy biomes. J Biogeogr. 2020; 47: 553-65.

[43]

Williams CA, Albertson JD . Dynamical effects of the statistical structure of annual rainfall on dryland vegetation. Glob Chang Biol. 2006; 12: 777-92.

[44]

Guo Q, Hu Z, Li S et al. Spatial variations in above-ground net primary productivity along a climate gradient in Eurasian temperate grassland: effects of mean annual precipitation and its seasonal distribution. Glob Chang Biol. 2012; 18: 3624-31.

[45]

Jiang Y, Ownley BH, Chen F . Terpenoids from weedy rice-field flatsedge (Cyperus iria L.) are developmentally regulated and stress-induced, and have antifungal properties . Molecules. 2018; 23: 3149.

[46]

Chen F, Tholl D, D’Auria JC et al. Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. Plant Cell. 2003; 15: 481-94.

[47]

Chen F, al-Ahmad H, Joyce B et al. Within-plant distribution and emission of sesquiterpenes from Copaifera officinalis . Plant Physiol Biochem. 2009; 47: 1017-23.

[48]

Muldashev AA . A new genus Phaeostigma (Asteraceae) from the East Asia. Botanischeskii Zhurnal. 1981; 66: 584-8.

[49]

Bremer K, Humphries CJ . Generic monograph of the Asteraceae-Anthemideae. Bull Nat Hist Mus London (Botany). 1993; 23: 71-177.

[50]

Ohashi H, Yonekura K . New combinations in Chrysanthemum (Compositae-Anthemideae) of Asia with a list of Japanese species. J Japanese Bot. 2004; 79: 186-95.

[51]

Shi ZN, Wu HR, Pang XY et al. Secondary metabolites from Ajania salicifolia and their chemotaxonomic significance. Biochem Syst Ecol. 2017; 70: 162-7.

[52]

Ma YP, Chen MM, Wei JX et al. Origin of Chrysanthemum cultivars - evidence from nuclear low-copy LFY gene sequences . Biochem Syst Ecol. 2016; 65: 129-36.

[53]

Chen X, Wang H, Yang X et al. Small-scale alpine topography at low latitudes and high altitudes: refuge areas of the genus Chrysanthemum and its allies. Hortic Res. 2020; 7: 184.

[54]

Rohling EJ, Foster GL, Grant KM et al. Sea-level and deep-sea-temperature variability over the past 5.3 million years. Nature. 2014; 508: 477-82.

[55]

Jiao Y, Wickett NJ, Ayyampalayam S et al. Ancestral polyploidy in seed plants and angiosperms. Nature. 2011; 473: 97-100.

[56]

Schranz EM, Mohammadin S, Edger PP . Ancient whole genome duplications, novelty and diversification: the WGD radiation lag-time model. Curr Opin Plant Biol. 2012; 15: 147-53.

[57]

Huang CH, Zhang C, Liu M et al. Multiple polyploidization events across Asteraceae with two nested events in the early history revealed by nuclear phylogenomics. Mol Biol Evol. 2016; 33: 2820-35.

[58]

Rahbek C, Borregaard MK, Colwell RK et al. Humboldt’s enigma: what causes global patterns of mountain biodiversity? Science. 2019; 365: 1108-13.

[59]

Rahbek C, Borregaard MK, Antonelli A et al. Building mountain biodiversity: geological and evolutionary processes. Science. 2019; 365: 1114-9.

[60]

Xing Y, Ree RH . Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc Natl Acad Sci USA. 2017; 114: E3444.

[61]

Zhang DC, Zhang YH, Boufford DE et al. Elevational patterns of species richness and endemism for some important taxa in the Hengduan Mountains, southwestern China. Biodivers Conserv. 2009; 18: 699-716.

[62]

Shrestha N, Wang Z, Su X et al. Global patterns of rhododendron diversity: the role of evolutionary time and diversification rates. Glob Ecol Biogeogr. 2018; 27: 913-24.

[63]

Ding WN, Ree RH, Spicer RA et al. Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora. Science. 2020; 369: 578-81.

[64]

Zobel M, Otto R, Laanisto L et al. The formation of species pools: historical habitat abundance affects current local diversity. Glob Ecol Biogeogr. 2011; 20: 251-9.

[65]

Mandel JR, Dikow RB, Siniscalchi CM et al. A fully resolved backbone phylogeny reveals numerous dispersals and explosive diversifications throughout the history of Asteraceae. Proc Natl Acad Sci USA. 2019; 116: 14083-8.

[66]

Sheldon ND . Quaternary glacial-interglacial climate cycles in Hawaii. J Geol. 2006; 114: 367-76.

[67]

Shi X, Yao Z, Liu Q et al. Sedimentary architecture of the Bohai Sea China over the last 1 Ma and implications for sea-level changes. Earth Planet Sci Lett. 2016; 451: 10-21.

[68]

Ren L, Sun J, Chen S et al. A transcriptomic analysis of Chrysanthemum nankingense provides insights into the basis of low temperature tolerance. BMC Genomics. 2014; 15: 844.

[69]

Boufford DE . Fumaria. In: Flora of North America Editorial Committee (eds.) Flora of North America North of Mexico, Vol. 19. New York and Oxford. [Online] http://beta.floranorthamerica.org/Fumaria.

[70]

Hooker JD . Flora of British India (Volume III), LXXVIII. Compositae. 1882, 310-5.

[71]

Anderberg AA et al. The families and genera of vascular plants (Kubitzki K). In: VIII (Kadereit JW & Jeffrey C) Flowering Plants. Eudicots: Asterales . Berlin: Springer, 8, 2007, 357- 8.

[72]

Shih C, Peng GF, Zhang SQ et al. Two new species of the genus Dendranthema (DC.) des Moul. from China. Acta Phytotaxon Sin. 1999; 37: 598-600.

[73]

Shih C. A revision of Ajania potaninii (Krasch.) Poljak. group (Compositae) . Acta Phytotaxon Sin. 1994; 32: 365-8. [In Chinese with English abstract].

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