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Background <p>Plastome evolution in plants with diverse nutritional strategies provides unique insights into genomic-level adaptive processes. The genus <i>Cymbidium</i> (Orchidaceae), characterized by its heterogeneous life forms and transitions toward mycoheterotrophy, serves as an exemplary natural system for investigating chronospatial dynamics between ecological adaptation and plastomic evolutionary trajectories.</p> Results <p>In this study, plastomes and nrDNA datasets of 56 <i>Cymbidium</i> species (representing about 90% of all recognized species, encompassing 38 epiphytes and 18 terrestrials) were analyzed using phylogenomic, ancestral state reconstruction, and selection pressure tools (RELAX, aBSREL, BUSTED) to assess plastome structural variations, <i>ndh</i> pseudogenization, and evolutionary dynamics. Four inverted repeat (IR) boundary types were identified, with recurrent contractions linked to the <i>ndhF</i> gene loss, especially in terrestrial species (Type I/II). The <i>ndh</i> genes were functional in the ancestral state but underwent progressive degradation across both epiphytic (Clade II) and terrestrial (Clade III) lineages. The leafless <i>Cymbidium macrorhizon</i> exhibited delayed plastome degradation (retained 4 <i>ndh</i> genes) despite holomycoheterotrophy, reflecting recent divergence (~ 2.5&#xa0;Ma). Evolutionary selection analyses indicated the relaxed selection on certain genes and intensified selection on others, particularly within the <i>ndh</i> gene group. Phylogenetic incongruence was found between the plastome and nrDNA datasets, yet ancestral reconstructions remained consistent robustness.</p> Conclusions <p>Both epiphytic and terrestrial species experienced independent <i>ndh</i> degradation, likely reflecting adaptive responses to different ecological environments, not life form alone. Temporal decoupling of morphological-genomic evolution highlights plastome degradation lag in recent heterotrophic transitions. Integrating incongruent phylogenies strengthens evolutionary inferences, revealing conserved degradation trajectories across lineages.</p>

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Comprehensive species sampling reveals pervasive pseudogenization and recurrent complete loss of plastid ndh genes in the genus Cymbidium (Orchidaceae)

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2025年12月22日

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  • Hai-Yao Chen,
  • Li-Qiong Chen,
  • Xin Yao,
  • Zhi-Rong Zhang,
  • Ji-Dong Ya,
  • Xiao-Hua Jin,
  • De-Zhu Li,
  • Jun-Bo Yang,
  • Wen-Bin Yu

摘要

Background

Plastome evolution in plants with diverse nutritional strategies provides unique insights into genomic-level adaptive processes. The genus Cymbidium (Orchidaceae), characterized by its heterogeneous life forms and transitions toward mycoheterotrophy, serves as an exemplary natural system for investigating chronospatial dynamics between ecological adaptation and plastomic evolutionary trajectories.

Results

In this study, plastomes and nrDNA datasets of 56 Cymbidium species (representing about 90% of all recognized species, encompassing 38 epiphytes and 18 terrestrials) were analyzed using phylogenomic, ancestral state reconstruction, and selection pressure tools (RELAX, aBSREL, BUSTED) to assess plastome structural variations, ndh pseudogenization, and evolutionary dynamics. Four inverted repeat (IR) boundary types were identified, with recurrent contractions linked to the ndhF gene loss, especially in terrestrial species (Type I/II). The ndh genes were functional in the ancestral state but underwent progressive degradation across both epiphytic (Clade II) and terrestrial (Clade III) lineages. The leafless Cymbidium macrorhizon exhibited delayed plastome degradation (retained 4 ndh genes) despite holomycoheterotrophy, reflecting recent divergence (~ 2.5 Ma). Evolutionary selection analyses indicated the relaxed selection on certain genes and intensified selection on others, particularly within the ndh gene group. Phylogenetic incongruence was found between the plastome and nrDNA datasets, yet ancestral reconstructions remained consistent robustness.

Conclusions

Both epiphytic and terrestrial species experienced independent ndh degradation, likely reflecting adaptive responses to different ecological environments, not life form alone. Temporal decoupling of morphological-genomic evolution highlights plastome degradation lag in recent heterotrophic transitions. Integrating incongruent phylogenies strengthens evolutionary inferences, revealing conserved degradation trajectories across lineages.