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Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy

Ming-He Li, Ke-Wei Liu, Zhen Li (UGent) , Hsiang-Chia Lu, Qin-Liang Ye, Diyang Zhang, Jie-Yu Wang, Yu-Feng Li, Zhi-Ming Zhong, Xuedie Liu, et al.
(2022) NATURE PLANTS. 8(4). p.373-388
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Abstract
Analyses of the genome sequences and expression data for two closely related mycoheterotrophic orchid species provide insights into the genomic basis underlying the evolution of mycoheterotrophy. To improve our understanding of the origin and evolution of mycoheterotrophic plants, we here present the chromosome-scale genome assemblies of two sibling orchid species: partially mycoheterotrophic Platanthera zijinensis and holomycoheterotrophic Platanthera guangdongensis. Comparative analysis shows that mycoheterotrophy is associated with increased substitution rates and gene loss, and the deletion of most photoreceptor genes and auxin transporter genes might be linked to the unique phenotypes of fully mycoheterotrophic orchids. Conversely, trehalase genes that catalyse the conversion of trehalose into glucose have expanded in most sequenced orchids, in line with the fact that the germination of orchid non-endosperm seeds needs carbohydrates from fungi during the protocorm stage. We further show that the mature plant of P. guangdongensis, different from photosynthetic orchids, keeps expressing trehalase genes to hijack trehalose from fungi. Therefore, we propose that mycoheterotrophy in mature orchids is a continuation of the protocorm stage by sustaining the expression of trehalase genes. Our results shed light on the molecular mechanism underlying initial, partial and full mycoheterotrophy.
Keywords
Plant Science, NUCLEOTIDE SUBSTITUTION, EPIPOGIUM-APHYLLUM, SUPPLEMENT TREMBL, MYCO-HETEROTROPHY, SEQUENCE, CARBON, FUNGI, GENE, ALIGNMENT, NITROGEN

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MLA
Li, Ming-He, et al. “Genomes of Leafy and Leafless Platanthera Orchids Illuminate the Evolution of Mycoheterotrophy.” NATURE PLANTS, vol. 8, no. 4, 2022, pp. 373–88, doi:10.1038/s41477-022-01127-9.
APA
Li, M.-H., Liu, K.-W., Li, Z., Lu, H.-C., Ye, Q.-L., Zhang, D., … Liu, Z.-J. (2022). Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy. NATURE PLANTS, 8(4), 373–388. https://doi.org/10.1038/s41477-022-01127-9
Chicago author-date
Li, Ming-He, Ke-Wei Liu, Zhen Li, Hsiang-Chia Lu, Qin-Liang Ye, Diyang Zhang, Jie-Yu Wang, et al. 2022. “Genomes of Leafy and Leafless Platanthera Orchids Illuminate the Evolution of Mycoheterotrophy.” NATURE PLANTS 8 (4): 373–88. https://doi.org/10.1038/s41477-022-01127-9.
Chicago author-date (all authors)
Li, Ming-He, Ke-Wei Liu, Zhen Li, Hsiang-Chia Lu, Qin-Liang Ye, Diyang Zhang, Jie-Yu Wang, Yu-Feng Li, Zhi-Ming Zhong, Xuedie Liu, Xia Yu, Ding-Kun Liu, Xiong-De Tu, Bin Liu, Yang Hao, Xing-Yu Liao, Yu-Ting Jiang, Wei-Hong Sun, Jinliao Chen, Yan-Qiong Chen, Ye Ai, Jun-Wen Zhai, Sha-Sha Wu, Zhuang Zhou, Yu-Yun Hsiao, Wan-Lin Wu, You-Yi Chen, Yu-Fu Lin, Jui-Ling Hsu, Chia-Ying Li, Zhi-Wen Wang, Xiang Zhao, Wen-Ying Zhong, Xiao-Kai Ma, Liang Ma, Jie Huang, Gui-Zhen Chen, Ming-Zhong Huang, Laiqiang Huang, Dong-Hui Peng, Yi-Bo Luo, Shuang-Quan Zou, Shi-Pin Chen, Siren Lan, Wen-Chieh Tsai, Yves Van de Peer, and Zhong-Jian Liu. 2022. “Genomes of Leafy and Leafless Platanthera Orchids Illuminate the Evolution of Mycoheterotrophy.” NATURE PLANTS 8 (4): 373–388. doi:10.1038/s41477-022-01127-9.
Vancouver
1.
Li M-H, Liu K-W, Li Z, Lu H-C, Ye Q-L, Zhang D, et al. Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy. NATURE PLANTS. 2022;8(4):373–88.
IEEE
[1]
M.-H. Li et al., “Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy,” NATURE PLANTS, vol. 8, no. 4, pp. 373–388, 2022.
@article{8751563,
  abstract     = {{Analyses of the genome sequences and expression data for two closely related mycoheterotrophic orchid species provide insights into the genomic basis underlying the evolution of mycoheterotrophy.

To improve our understanding of the origin and evolution of mycoheterotrophic plants, we here present the chromosome-scale genome assemblies of two sibling orchid species: partially mycoheterotrophic Platanthera zijinensis and holomycoheterotrophic Platanthera guangdongensis. Comparative analysis shows that mycoheterotrophy is associated with increased substitution rates and gene loss, and the deletion of most photoreceptor genes and auxin transporter genes might be linked to the unique phenotypes of fully mycoheterotrophic orchids. Conversely, trehalase genes that catalyse the conversion of trehalose into glucose have expanded in most sequenced orchids, in line with the fact that the germination of orchid non-endosperm seeds needs carbohydrates from fungi during the protocorm stage. We further show that the mature plant of P. guangdongensis, different from photosynthetic orchids, keeps expressing trehalase genes to hijack trehalose from fungi. Therefore, we propose that mycoheterotrophy in mature orchids is a continuation of the protocorm stage by sustaining the expression of trehalase genes. Our results shed light on the molecular mechanism underlying initial, partial and full mycoheterotrophy.}},
  author       = {{Li, Ming-He and Liu, Ke-Wei and Li, Zhen and Lu, Hsiang-Chia and Ye, Qin-Liang and Zhang, Diyang and Wang, Jie-Yu and Li, Yu-Feng and Zhong, Zhi-Ming and Liu, Xuedie and Yu, Xia and Liu, Ding-Kun and Tu, Xiong-De and Liu, Bin and Hao, Yang and Liao, Xing-Yu and Jiang, Yu-Ting and Sun, Wei-Hong and Chen, Jinliao and Chen, Yan-Qiong and Ai, Ye and Zhai, Jun-Wen and Wu, Sha-Sha and Zhou, Zhuang and Hsiao, Yu-Yun and Wu, Wan-Lin and Chen, You-Yi and Lin, Yu-Fu and Hsu, Jui-Ling and Li, Chia-Ying and Wang, Zhi-Wen and Zhao, Xiang and Zhong, Wen-Ying and Ma, Xiao-Kai and Ma, Liang and Huang, Jie and Chen, Gui-Zhen and Huang, Ming-Zhong and Huang, Laiqiang and Peng, Dong-Hui and Luo, Yi-Bo and Zou, Shuang-Quan and Chen, Shi-Pin and Lan, Siren and Tsai, Wen-Chieh and Van de Peer, Yves and Liu, Zhong-Jian}},
  issn         = {{2055-026X}},
  journal      = {{NATURE PLANTS}},
  keywords     = {{Plant Science,NUCLEOTIDE SUBSTITUTION,EPIPOGIUM-APHYLLUM,SUPPLEMENT TREMBL,MYCO-HETEROTROPHY,SEQUENCE,CARBON,FUNGI,GENE,ALIGNMENT,NITROGEN}},
  language     = {{eng}},
  number       = {{4}},
  pages        = {{373--388}},
  title        = {{Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy}},
  url          = {{http://doi.org/10.1038/s41477-022-01127-9}},
  volume       = {{8}},
  year         = {{2022}},
}
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