The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence

Xiong Huang; Wenling Wang; Ting Gong; David Wickell; Li-Yaung Kuo; Xingtan Zhang; Jialong Wen; Hoon Kim; Fachuang Lu; Hansheng Zhao; Song Chen; Hui Li; Wenqi Wu; Changjiang Yu; Su Chen; Wei Fan; Shuai Chen; Xiuqi Bao; Li Li; Dan Zhang; Longyu Jiang; Dipak Khadka; Xiaojing Yan; Zhenyang Liao; Gongke Zhou; Yalong Guo; John Ralph; Ronald R Sederoff; Hairong Wei; Ping Zhu; Fay-Wei Li; Ray Ming; Quanzi Li

doi:10.1038/s41477-022-01146-6

The flying spider-monkey tree fern genome provides insights into fern evolution and arborescence

Nat Plants. 2022 May;8(5):500-512. doi: 10.1038/s41477-022-01146-6. Epub 2022 May 9.

Authors

Xiong Huang^#¹, Wenling Wang^#², Ting Gong^#³, David Wickell^#^{4

5}, Li-Yaung Kuo⁶, Xingtan Zhang², Jialong Wen⁷, Hoon Kim⁸, Fachuang Lu⁸, Hansheng Zhao⁹, Song Chen¹⁰, Hui Li¹, Wenqi Wu¹¹, Changjiang Yu¹², Su Chen¹⁰, Wei Fan¹, Shuai Chen², Xiuqi Bao³, Li Li³, Dan Zhang³, Longyu Jiang³, Dipak Khadka¹³, Xiaojing Yan¹, Zhenyang Liao², Gongke Zhou¹², Yalong Guo¹⁴, John Ralph⁸, Ronald R Sederoff¹⁵, Hairong Wei¹⁶, Ping Zhu¹⁷, Fay-Wei Li^{18

19}, Ray Ming²⁰, Quanzi Li²¹

Affiliations

¹ State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, China.
² Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China.
³ State Key Laboratory of Bioactive Substance and Function of Natural Medicines; NHC Key Laboratory of Biosynthesis of Natural Products; CAMS Key Laboratory of Enzyme and Biocatalysis of Natural Drugs, Institute of Materia Medica, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China.
⁴ Thompson Institute, Ithaca, NY, USA.
⁵ Plant Biology Section, Cornell University, Ithaca, NY, USA.
⁶ Institute of Molecular & Cellular Biology, National Tsing Hua University, Hsinchu, Taiwan.
⁷ Beijing Key Laboratory of Lignocellulosic Chemistry, Beijing Forestry University, Beijing, China.
⁸ Department of Biochemistry and DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, University of Wisconsin, Madison, WI, USA.
⁹ State Forestry Administration Key Open Laboratory on the Science and Technology of Bamboo and Rattan, Institute of Gene for Bamboo and Rattan Resources, International Center for Bamboo and Rattan, Beijing, China.
¹⁰ State Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, China.
¹¹ Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, Beijing, China.
¹² College of Landscape Architecture and Forestry, Qingdao Agricultural University, Qingdao, China.
¹³ GoldenGate International College, Tribhuvan University, Battisputali, Kathmandu, Nepal.
¹⁴ State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Science, Beijing, China.
¹⁵ Forest Biotechnology Group, Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC, USA.
¹⁶ College of Forest Resources and Environmental Science, Michigan Technological University, Houghton, MI, USA. hairong@mtu.edu.
¹⁷ State Key Laboratory of Bioactive Substance and Function of Natural Medicines; NHC Key Laboratory of Biosynthesis of Natural Products; CAMS Key Laboratory of Enzyme and Biocatalysis of Natural Drugs, Institute of Materia Medica, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, China. zhuping@imm.ac.cn.
¹⁸ Thompson Institute, Ithaca, NY, USA. fl329@cornell.edu.
¹⁹ Plant Biology Section, Cornell University, Ithaca, NY, USA. fl329@cornell.edu.
²⁰ Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA. rayming@illinois.edu.
²¹ State Key Laboratory of Tree Genetics and Breeding, Chinese Academy of Forestry, Beijing, China. liqz@caf.ac.cn.

^# Contributed equally.

Abstract

To date, little is known about the evolution of fern genomes, with only two small genomes published from the heterosporous Salviniales. Here we assembled the genome of Alsophila spinulosa, known as the flying spider-monkey tree fern, onto 69 pseudochromosomes. The remarkable preservation of synteny, despite resulting from an ancient whole-genome duplication over 100 million years ago, is unprecedented in plants and probably speaks to the uniqueness of tree ferns. Our detailed investigations into stem anatomy and lignin biosynthesis shed new light on the evolution of stem formation in tree ferns. We identified a phenolic compound, alsophilin, that is abundant in xylem, and we provided the molecular basis for its biosynthesis. Finally, analysis of demographic history revealed two genetic bottlenecks, resulting in rapid demographic declines of A. spinulosa. The A. spinulosa genome fills a crucial gap in the plant genomic landscape and helps elucidate many unique aspects of tree fern biology.

MeSH terms

Animals
Atelinae* / genetics
Ferns* / genetics
Genome, Plant
Phylogeny
Spiders* / genetics