Genome size evolution of the extant lycophytes and ferns

doi:10.1016/j.pld.2021.11.007

Plant Diversity ›› 2022, Vol. 44 ›› Issue (02): 141-152.DOI: 10.1016/j.pld.2021.11.007

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Genome size evolution of the extant lycophytes and ferns

Fa-Guo Wang^a, Ai-Hua Wang^a,d, Cheng-Ke Bai^b, Dong-Mei Jin^c, Li-Yun Nie^a, AJ Harris^a,e, Le Che^b, Juan-Juan Wang^b, Shi-Yu Li^a, Lei Xu^a, Hui Shen^c, Yu-Feng Gu^c,g,h, Hui Shang^c, Lei Duan^a, Xian-Chun Zhang^f, Hong-Feng Chen^a, Yue-Hong Yan^c,g

a Key Laboratory of Plant Resources Conservation and Sustainable Utilization, Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China;
b College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, China;
c Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, 201602, China;
d Key Laboratory of Environment Change and Resources Use in Beibu Gulf, Ministry of Education, Nanning Normal University, Nanning, 530001, China;
e Department of Biology, Oberlin College, Oberlin, OH, 44074, USA;
f State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China;
g Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, the National Orchid Conservation Center of China and the Orchid Conservation & Research Center of Shenzhen, 518114, Shenzhen, China;
h Life Science and Technology College, Harbin Normal University, Harbin, 150025, China

Received:2021-04-11 Revised:2021-11-24 Online:2022-04-24 Published:2022-04-25
Contact: Hong-Feng Chen,E-mail:h.f.chen@scbg.ac.cn;Yue-Hong Yan,E-mail:yhyan@sibs.ac.cn
Supported by:
We thank Yu-Wen Cui for his assistance with data collection and analyses in R. This research was supported by the National Natural Science Foundation of China (grant number 31870188, 31800174, 31700172, 41571056) to Wang, Shen, Wang and Xing, Shanghai Landscaping and City Appearance Administrative Bureau of China, Scientific Research Grants (G182411) to Yan, the Strategic Priority Research Program of the Chinese Academy of Sciences (grant number XDA13020603, XDA13020500) to Chen and Jian, Guangdong Natural Science Foundation (grant number 2015A030308015) to Wang.

Genome size evolution of the extant lycophytes and ferns

a Key Laboratory of Plant Resources Conservation and Sustainable Utilization, Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China;
b College of Life Sciences, Shaanxi Normal University, Xi'an, 710062, China;
c Eastern China Conservation Centre for Wild Endangered Plant Resources, Shanghai Chenshan Botanical Garden, Shanghai, 201602, China;
d Key Laboratory of Environment Change and Resources Use in Beibu Gulf, Ministry of Education, Nanning Normal University, Nanning, 530001, China;
e Department of Biology, Oberlin College, Oberlin, OH, 44074, USA;
f State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China;
g Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, the National Orchid Conservation Center of China and the Orchid Conservation & Research Center of Shenzhen, 518114, Shenzhen, China;
h Life Science and Technology College, Harbin Normal University, Harbin, 150025, China

通讯作者: Hong-Feng Chen,E-mail:h.f.chen@scbg.ac.cn;Yue-Hong Yan,E-mail:yhyan@sibs.ac.cn
基金资助:
We thank Yu-Wen Cui for his assistance with data collection and analyses in R. This research was supported by the National Natural Science Foundation of China (grant number 31870188, 31800174, 31700172, 41571056) to Wang, Shen, Wang and Xing, Shanghai Landscaping and City Appearance Administrative Bureau of China, Scientific Research Grants (G182411) to Yan, the Strategic Priority Research Program of the Chinese Academy of Sciences (grant number XDA13020603, XDA13020500) to Chen and Jian, Guangdong Natural Science Foundation (grant number 2015A030308015) to Wang.

Abstract

Abstract: Ferns and lycophytes have remarkably large genomes. However, little is known about how their genome size evolved in fern lineages. To explore the origins and evolution of chromosome numbers and genome size in ferns, we used flow cytometry to measure the genomes of 240 species (255 samples) of extant ferns and lycophytes comprising 27 families and 72 genera, of which 228 species (242 samples) represent new reports. We analyzed correlations among genome size, spore size, chromosomal features, phylogeny, and habitat type preference within a phylogenetic framework. We also applied ANOVA and multinomial logistic regression analysis to preference of habitat type and genome size. Using the phylogeny, we conducted ancestral character reconstruction for habitat types and tested whether genome size changes simultaneously with shifts in habitat preference. We found that 2C values had weak phylogenetic signal, whereas the base number of chromosomes (x) had a strong phylogenetic signal. Furthermore, our analyses revealed a positive correlation between genome size and chromosome traits, indicating that the base number of chromosomes (x), chromosome size, and polyploidization may be primary contributors to genome expansion in ferns and lycophytes. Genome sizes in different habitat types varied significantly and were significantly correlated with habitat types; specifically, multinomial logistic regression indicated that species with larger 2C values were more likely to be epiphytes. Terrestrial habitat is inferred to be ancestral for both extant ferns and lycophytes, whereas transitions to other habitat types occurred as the major clades emerged. Shifts in habitat types appear be followed by periods of genomic stability. Based on these results, we inferred that habitat type changes and multiple whole-genome duplications have contributed to the formation of large genomes of ferns and their allies during their evolutionary history.

Key words: Genome size, Ferns, Chromosome numbers, Habitat type, Whole-genome duplications, Evolution

摘要： Ferns and lycophytes have remarkably large genomes. However, little is known about how their genome size evolved in fern lineages. To explore the origins and evolution of chromosome numbers and genome size in ferns, we used flow cytometry to measure the genomes of 240 species (255 samples) of extant ferns and lycophytes comprising 27 families and 72 genera, of which 228 species (242 samples) represent new reports. We analyzed correlations among genome size, spore size, chromosomal features, phylogeny, and habitat type preference within a phylogenetic framework. We also applied ANOVA and multinomial logistic regression analysis to preference of habitat type and genome size. Using the phylogeny, we conducted ancestral character reconstruction for habitat types and tested whether genome size changes simultaneously with shifts in habitat preference. We found that 2C values had weak phylogenetic signal, whereas the base number of chromosomes (x) had a strong phylogenetic signal. Furthermore, our analyses revealed a positive correlation between genome size and chromosome traits, indicating that the base number of chromosomes (x), chromosome size, and polyploidization may be primary contributors to genome expansion in ferns and lycophytes. Genome sizes in different habitat types varied significantly and were significantly correlated with habitat types; specifically, multinomial logistic regression indicated that species with larger 2C values were more likely to be epiphytes. Terrestrial habitat is inferred to be ancestral for both extant ferns and lycophytes, whereas transitions to other habitat types occurred as the major clades emerged. Shifts in habitat types appear be followed by periods of genomic stability. Based on these results, we inferred that habitat type changes and multiple whole-genome duplications have contributed to the formation of large genomes of ferns and their allies during their evolutionary history.

关键词: Genome size, Ferns, Chromosome numbers, Habitat type, Whole-genome duplications, Evolution

Fa-Guo Wang, Ai-Hua Wang, Cheng-Ke Bai, Dong-Mei Jin, Li-Yun Nie, AJ Harris, Le Che, Juan-Juan Wang, Shi-Yu Li, Lei Xu, Hui Shen, Yu-Feng Gu, Hui Shang, Lei Duan, Xian-Chun Zhang, Hong-Feng Chen, Yue-Hong Yan. Genome size evolution of the extant lycophytes and ferns[J]. Plant Diversity, 2022, 44(02): 141-152.

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Genome size evolution of the extant lycophytes and ferns

Genome size evolution of the extant lycophytes and ferns

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