Ecophysiological transition mediated by hybridization in a hybrid pine species complex

doi:10.1016/j.pld.2025.05.009

Plant Diversity ›› 2025, Vol. 47 ›› Issue (04): 604-619.DOI: 10.1016/j.pld.2025.05.009

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Ecophysiological transition mediated by hybridization in a hybrid pine species complex

Zhi-Chao Li^a, Chao-Qun Xu^a,b, Wei Zhao^c, Shuai Nie^a,d, Yu-Tao Bao^a, Hui Liu^c, Zhen Xing^e, Jian-Feng Mao^a,f, Xiao-Ru Wang^a,c

a. State Key Laboratory of Tree Genetics and Breeding, National Engineering Research Center of Tree Breeding and Ecological Restoration, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China;
b. Key Laboratory of Bioactive Substances and Resources Utilization of Chinese Herbal Medicines, Ministry of Education, Institute of Medicinal Plant Development, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing 100193, China;
c. Department of Ecology and Environmental Science, Umeå Plant Science Centre, Umeå University, SE-901 87 Umeå, Sweden;
d. Rice Research Institute, Guangdong Academy of Agricultural Sciences & Key Laboratory of Genetics and Breeding of High Quality Rice in Southern China (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs & Guangdong Key Laboratory of New Technology in Rice Breeding, Guangzhou 510640, China;
e. Resources and Environmental College, Xizang Agriculture and Animal Husbandry University, Linzhi, Xizang, 860000, China;
f. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, SE-90187 Umeå, Sweden

Received:2025-02-24 Revised:2025-04-22 Online:2025-08-13 Published:2025-08-13
Contact: Jian-Feng Mao,E-mail:jianfeng.mao@umu.se;Xiao-Ru Wang,E-mail:xiao-ru.wang@umu.se
Supported by:
This study was supported by the National Natural Science Foundation of China (32171816), and T4F program Sweden.

Ecophysiological transition mediated by hybridization in a hybrid pine species complex

Zhi-Chao Li^a, Chao-Qun Xu^a,b, Wei Zhao^c, Shuai Nie^a,d, Yu-Tao Bao^a, Hui Liu^c, Zhen Xing^e, Jian-Feng Mao^a,f, Xiao-Ru Wang^a,c

a. State Key Laboratory of Tree Genetics and Breeding, National Engineering Research Center of Tree Breeding and Ecological Restoration, National Engineering Laboratory for Tree Breeding, Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China;
b. Key Laboratory of Bioactive Substances and Resources Utilization of Chinese Herbal Medicines, Ministry of Education, Institute of Medicinal Plant Development, Peking Union Medical College and Chinese Academy of Medical Sciences, Beijing 100193, China;
c. Department of Ecology and Environmental Science, Umeå Plant Science Centre, Umeå University, SE-901 87 Umeå, Sweden;
d. Rice Research Institute, Guangdong Academy of Agricultural Sciences & Key Laboratory of Genetics and Breeding of High Quality Rice in Southern China (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs & Guangdong Key Laboratory of New Technology in Rice Breeding, Guangzhou 510640, China;
e. Resources and Environmental College, Xizang Agriculture and Animal Husbandry University, Linzhi, Xizang, 860000, China;
f. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, SE-90187 Umeå, Sweden

通讯作者: Jian-Feng Mao,E-mail:jianfeng.mao@umu.se;Xiao-Ru Wang,E-mail:xiao-ru.wang@umu.se
基金资助:
This study was supported by the National Natural Science Foundation of China (32171816), and T4F program Sweden.

Abstract

Abstract: Hybridization is a driving force in ecological transitions and speciation, yet direct evidence linking it to adaptive differentiation in natural systems remains limited. This study evaluates the role of hybridization in the speciation of Pinus densata, a keystone forest species on the southeastern Tibetan Plateau. By creating artificial interspecific F1s and a long-term common garden experiment on the plateau, we provide in situ assessments on 44 growth and physiological traits across four seasons, along with RNA sequencing. We found significant phenotypic divergence between P. densata and its putative parental species P. tabuliformis and P. yunnanensis, with P. densata demonstrating superior growth and dynamic balance between photosynthesis and photoprotection. The F1s closely resembled P. densata in most traits. Gene expression revealed 19%–10% of 34,000 examined genes as differentially expressed in P. densata and F1s relative to mid-parent expression values. Both additive (4%) and non-additive gene actions (5%–6% in F1s, 10%–12% in P. densata) were common, while transgressive expression occurred more frequently in the stabilized natural hybrids, illustrating transcriptomic reprogramming brought by hybridization and further divergence by natural selection. We provide compelling evidence for hybridization-derived phenotypic divergence at both physiological and gene expression levels that could have contributed to the adaptation of P. densata to high plateau habitat where both parental species have low fitness. The altered physiology and gene expression in hybrids serve both as a substrate for novel ecological adaptation and as a mechanism for the initiation of reproductive isolation.

Key words: Ecological divergence, Gene action, Homoploid hybrid speciation, Physiological traits, RNA-Seq, Tibetan plateau

摘要： Hybridization is a driving force in ecological transitions and speciation, yet direct evidence linking it to adaptive differentiation in natural systems remains limited. This study evaluates the role of hybridization in the speciation of Pinus densata, a keystone forest species on the southeastern Tibetan Plateau. By creating artificial interspecific F1s and a long-term common garden experiment on the plateau, we provide in situ assessments on 44 growth and physiological traits across four seasons, along with RNA sequencing. We found significant phenotypic divergence between P. densata and its putative parental species P. tabuliformis and P. yunnanensis, with P. densata demonstrating superior growth and dynamic balance between photosynthesis and photoprotection. The F1s closely resembled P. densata in most traits. Gene expression revealed 19%–10% of 34,000 examined genes as differentially expressed in P. densata and F1s relative to mid-parent expression values. Both additive (4%) and non-additive gene actions (5%–6% in F1s, 10%–12% in P. densata) were common, while transgressive expression occurred more frequently in the stabilized natural hybrids, illustrating transcriptomic reprogramming brought by hybridization and further divergence by natural selection. We provide compelling evidence for hybridization-derived phenotypic divergence at both physiological and gene expression levels that could have contributed to the adaptation of P. densata to high plateau habitat where both parental species have low fitness. The altered physiology and gene expression in hybrids serve both as a substrate for novel ecological adaptation and as a mechanism for the initiation of reproductive isolation.

关键词: Ecological divergence, Gene action, Homoploid hybrid speciation, Physiological traits, RNA-Seq, Tibetan plateau

Zhi-Chao Li, Chao-Qun Xu, Wei Zhao, Shuai Nie, Yu-Tao Bao, Hui Liu, Zhen Xing, Jian-Feng Mao, Xiao-Ru Wang. Ecophysiological transition mediated by hybridization in a hybrid pine species complex[J]. Plant Diversity, 2025, 47(04): 604-619.

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Ecophysiological transition mediated by hybridization in a hybrid pine species complex

Ecophysiological transition mediated by hybridization in a hybrid pine species complex

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