Dissecting mitogenomic conflict to illuminate angiosperm deep phylogeny: Sequence and architectural evidence

doi:10.1016/j.pld.2025.10.003

Plant Diversity ›› 2026, Vol. 48 ›› Issue (01): 41-58.DOI: 10.1016/j.pld.2025.10.003

Dissecting mitogenomic conflict to illuminate angiosperm deep phylogeny: Sequence and architectural evidence

Liyun Nie^a,b,c, Jie Wang^a,b,c, Lei Huang^d, Jiali Kong^a,b, Bao Nie^a,b, Luke R. Tembrock^e, Shanshan Dong^f, Ravi Tiwari^c, Hui Wang^f, Shenglong Kan^a,g, Xinhui Zou^h, Zhiqiang Wu^a,b,c

a Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518020, China;
b State Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518020, China;
c School of Medical, Molecular and Forensic Sciences, Murdoch University, Murdoch 6149, WA, Australia;
d National Engineering Laboratory for Resource Development of Endangered Crude Drugs in Northwest China, College of Life Sciences, Shaanxi Normal University, Xi'an 710119, Shaanxi, China;
e Department of Agricultural Biology, Colorado State University, Fort Collins, CO 80523, USA;
f Shenzhen Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen 518004, Guangdong, China;
g Marine College, Shandong University, Weihai 264209, Shandong, China;
h. State Key Laboratory of Plant Diversity and Specialty Crops and Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

收稿日期:2025-07-14 修回日期:2025-10-20 出版日期:2026-01-25 发布日期:2026-03-05
通讯作者: Hui Wang,E-mail:wanghui661@foxmail.com;Shenglong Kan,E-mail:kanshenglong@sdu.edu.cn;Xinhui Zou,E-mail:zouxh@ibcas.ac.cn;Zhiqiang Wu,E-mail:wuzhiqiang@caas.cn
基金资助:
This work was funded by the Shenzhen Science and Technology Program (Grant No. JCYJ20241202130723030); the National Natural Science Foundation of China (Grant No. 32170238); the Guangdong Pearl River Talent Program (Grant No. 2021QN02N792); the Shenzhen Fundamental Research Program (Grant No. JCYJ20220818103212025); the Chinese Academy of Agricultural Sciences Elite Youth Program (110243160001007) to Z.W.

Dissecting mitogenomic conflict to illuminate angiosperm deep phylogeny: Sequence and architectural evidence

Liyun Nie^a,b,c, Jie Wang^a,b,c, Lei Huang^d, Jiali Kong^a,b, Bao Nie^a,b, Luke R. Tembrock^e, Shanshan Dong^f, Ravi Tiwari^c, Hui Wang^f, Shenglong Kan^a,g, Xinhui Zou^h, Zhiqiang Wu^a,b,c

a Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518020, China;
b State Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518020, China;
c School of Medical, Molecular and Forensic Sciences, Murdoch University, Murdoch 6149, WA, Australia;
d National Engineering Laboratory for Resource Development of Endangered Crude Drugs in Northwest China, College of Life Sciences, Shaanxi Normal University, Xi'an 710119, Shaanxi, China;
e Department of Agricultural Biology, Colorado State University, Fort Collins, CO 80523, USA;
f Shenzhen Key Laboratory of Southern Subtropical Plant Diversity, Fairy Lake Botanical Garden, Shenzhen & Chinese Academy of Sciences, Shenzhen 518004, Guangdong, China;
g Marine College, Shandong University, Weihai 264209, Shandong, China;
h. State Key Laboratory of Plant Diversity and Specialty Crops and Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

Received:2025-07-14 Revised:2025-10-20 Online:2026-01-25 Published:2026-03-05
Contact: Hui Wang,E-mail:wanghui661@foxmail.com;Shenglong Kan,E-mail:kanshenglong@sdu.edu.cn;Xinhui Zou,E-mail:zouxh@ibcas.ac.cn;Zhiqiang Wu,E-mail:wuzhiqiang@caas.cn
Supported by:
This work was funded by the Shenzhen Science and Technology Program (Grant No. JCYJ20241202130723030); the National Natural Science Foundation of China (Grant No. 32170238); the Guangdong Pearl River Talent Program (Grant No. 2021QN02N792); the Shenzhen Fundamental Research Program (Grant No. JCYJ20220818103212025); the Chinese Academy of Agricultural Sciences Elite Youth Program (110243160001007) to Z.W.

摘要/Abstract

摘要： Deep relationships in the angiosperm tree of life remain highly controversial. To address this, we first assembled the complete mitochondrial genomes for Ceratophyllum demersum and Chloranthus sessilifolius, confirming a well-supported sister relationship that starkly conflicts with nuclear and plastid data. To dissect this classic cyto-nuclear conflict, we developed the ‘PhyloForensics’ framework, a novel diagnostic approach to systematically identify sources of phylogenetic instability. This framework revealed that signal heterogeneity (topological entropy variance) and information content (the proportion of informative sites) are the primary drivers of gene-tree conflict. Empirically validating this, we show that removing a small subset of “loudly conflicted” genes resolves deep-level incongruence, yielding a single, highly-supported topology previously obscured by noise. Finally, complementing this sequence-based resolution, we demonstrate that mitogenome architecture provides powerful phylogenetic signals, revealing predictable, mitogenome-wide evolutionary patterns, such as a significant negative correlation between branch length and both GC content and RNA editing sites. By integrating a validated conflict-resolution framework with architectural genomics, our study provides a comprehensive strategy for navigating the complexities of deep evolutionary histories.

关键词: Angiosperm phylogeny, Ceratophyllales, Chloranthales, Evolutionary correlation, Mitochondrial genomes

Abstract: Deep relationships in the angiosperm tree of life remain highly controversial. To address this, we first assembled the complete mitochondrial genomes for Ceratophyllum demersum and Chloranthus sessilifolius, confirming a well-supported sister relationship that starkly conflicts with nuclear and plastid data. To dissect this classic cyto-nuclear conflict, we developed the ‘PhyloForensics’ framework, a novel diagnostic approach to systematically identify sources of phylogenetic instability. This framework revealed that signal heterogeneity (topological entropy variance) and information content (the proportion of informative sites) are the primary drivers of gene-tree conflict. Empirically validating this, we show that removing a small subset of “loudly conflicted” genes resolves deep-level incongruence, yielding a single, highly-supported topology previously obscured by noise. Finally, complementing this sequence-based resolution, we demonstrate that mitogenome architecture provides powerful phylogenetic signals, revealing predictable, mitogenome-wide evolutionary patterns, such as a significant negative correlation between branch length and both GC content and RNA editing sites. By integrating a validated conflict-resolution framework with architectural genomics, our study provides a comprehensive strategy for navigating the complexities of deep evolutionary histories.

Key words: Angiosperm phylogeny, Ceratophyllales, Chloranthales, Evolutionary correlation, Mitochondrial genomes

Liyun Nie, Jie Wang, Lei Huang, Jiali Kong, Bao Nie, Luke R. Tembrock, Shanshan Dong, Ravi Tiwari, Hui Wang, Shenglong Kan, Xinhui Zou, Zhiqiang Wu. Dissecting mitogenomic conflict to illuminate angiosperm deep phylogeny: Sequence and architectural evidence[J]. Plant Diversity, 2026, 48(01): 41-58.

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Dissecting mitogenomic conflict to illuminate angiosperm deep phylogeny: Sequence and architectural evidence

Dissecting mitogenomic conflict to illuminate angiosperm deep phylogeny: Sequence and architectural evidence

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