Molecular phylogenetic relationships based on chloroplast genomes of Zingiberaceae species: Insights into evolution and adaptation to extreme environments.

IF 4.1 2区 生物学 Q1 PLANT SCIENCES
Frontiers in Plant Science Pub Date : 2025-09-24 eCollection Date: 2025-01-01 DOI:10.3389/fpls.2025.1670568
Tian Lu, Yebing Yin, Jinglin Luo, Jiao Chen, Yu Wu, Wu Zhang, Yiling Wei, Tao Yuan
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引用次数: 0

Abstract

Introduction: The Zingiberaceae family, which includes numerous economically and medicinally important species, exhibits considerable phylogenetic and genetic diversity. Chloroplast genomes are valuable resources for studying evolutionary relationships, genetic diversity, and adaptive evolution in plants. While many Zingiberaceae chloroplast genomes have been sequenced, the evolutionary mechanisms-including structural variation, codon usage bias, selection pressures, and divergence history-remain to be comprehensively investigated.

Methods: we performed a comparative analysis of 11 newly identified species (Aframomum alboviolaceum, Amomum longipetiolatum, Amomum petaloideum, Amomum velutinum, Cautleya spicata, Cornukaempferia larsenii, Globba atrosanguinea, Globba variabilis, Hedychium aureum, Riedelia arfakensis, and Zingiber citriodorum) and 110 published data from the Zingiberaceae family, including their structure, codon usage, nucleotide polymorphisms, divergence time, and selection pressures.

Results: The chloroplast genomes of Zingiberaceae species exhibited a highly conserved structure with no significant expansion or contraction during diversification. Analysis revealed four hypervariable protein-coding genes (atpH, rpl32, ndhA, and ycf1) and one intergenic region (psac-ndhE), which are proposed as potential molecular markers for future phylogeographic and population genetic studies. Codon usage bias was found to be predominantly shaped by natural selection. Phylogenetic analysis strongly supported the division of Zingiberaceae into two primary subfamilies (Alpinioideae and Zingiberoideae) and clarified key relationships, revealing that Globba is more closely related to Curcuma than to Hedychium, and Hedychium is more closely related to the Pommereschea-Rhynchanthus clade than to Cautleya. Divergence time estimation indicated two rapid diversification events within Zingiberoideae, coinciding with the rapid uplift of the Tibetan Plateau and a Late Miocene cooling event linked to declining CO₂ levels. Ancestral range reconstruction suggested an African origin during the Cretaceous period, followed by dispersal to Southeast Asia and India. Selection pressure analysis showed that most protein-coding genes are under negative selection. In contrast, the ycf2 gene was found to be under relaxed selection. Furthermore, two genes (matK and ndhB) were identified to be under positive selection in high-altitude species of Roscoea, suggesting a role in adaptation to alpine environments.

Discussion: This study provides a comprehensive genomic analysis of the Zingiberaceae family, highlighting the conserved nature of chloroplast genome structure despite extensive diversification. The identified mutation hotspots present valuable tools for developing high-resolution markers for species identification and biogeographic studies. The phylogenetic results resolve longstanding uncertainties in the relationships among key genera. The inferred divergence times and ancestral range suggest that the evolutionary history of Zingiberaceae was significantly influenced by major geological and climatic events, notably the uplift of the Tibetan Plateau and global cooling in the Late Miocene. The prevalence of negative/purifying selection across most genes indicates strong evolutionary constraints to maintain core photosynthetic functions. The discovery of positively selected genes in high-altitude Roscoea species provides insights into adaptive evolution to environmental stressors. These findings offer foundational knowledge for future efforts in crop improvement, species identification, and the conservation of genetic diversity within the Zingiberaceae family.

基于姜科植物叶绿体基因组的分子系统发育关系:对极端环境的进化和适应的见解。
姜科包括许多重要的经济和药用物种,具有相当大的系统发育和遗传多样性。叶绿体基因组是研究植物进化关系、遗传多样性和适应性进化的宝贵资源。虽然许多姜科叶绿体基因组已被测序,但其进化机制,包括结构变异、密码子使用偏倚、选择压力和分化历史,仍有待全面研究。方法:对11个新鉴定种(阿夫拉蒙(Aframomum alboviolaceum)、长叶砂(Amomum longipetiolatum)、花瓣砂(Amomum petaloideum)、绒砂(Amomum velutinum)、细穗蒿(Cautleya spicata)、大角蒿(Cornukaempferia larsenii)、atrosanguinea、Globba variabilis、金缕草(Hedychium aureum)、Riedelia arfakensis和柠檬姜(Zingiber citriodorum))与110份已发表的姜科植物资料进行了结构、密码子使用、核苷酸多态性、分化时间和选择压力等方面的比较分析。结果:姜科植物叶绿体基因组在多样化过程中呈现高度保守的结构,没有明显的扩张或收缩。分析发现了4个高变蛋白编码基因(atpH、rpl32、ndhA和ycf1)和1个基因间区(psac-ndhE),这些基因间区被认为是未来系统地理和群体遗传研究的潜在分子标记。密码子使用偏差主要是由自然选择形成的。系统发育分析有力地支持了姜科植物分为两个主要亚科(Alpinioideae和Zingiberoideae),并明确了关键关系,揭示了Globba与Curcuma的亲缘关系比与Hedychium的亲缘关系更近,Hedychium与Pommereschea-Rhynchanthus分支的亲缘关系比与Cautleya的亲缘关系更近。祖先范围重建表明白垩纪时期起源于非洲,随后分散到东南亚和印度。选择压力分析表明,大多数蛋白质编码基因处于负选择状态。而ycf2基因则处于宽松选择状态。此外,在高海拔物种中鉴定出两个基因(matK和ndhB)处于正选择状态,提示其在适应高山环境中起作用。讨论:本研究对姜科植物进行了全面的基因组分析,强调了尽管广泛多样化,但叶绿体基因组结构的保守性。发现的突变热点为开发高分辨率的物种鉴定和生物地理研究标记提供了有价值的工具。系统发育结果解决了长期以来关键属之间关系的不确定性。在大多数基因中普遍存在的负选择/纯化选择表明,维持核心光合作用的进化限制很强。高海拔罗斯科物种中正选择基因的发现提供了对环境压力源的适应性进化的见解。这些发现为姜科植物的作物改良、物种鉴定和遗传多样性保护提供了基础知识。
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来源期刊
Frontiers in Plant Science
Frontiers in Plant Science PLANT SCIENCES-
CiteScore
7.30
自引率
14.30%
发文量
4844
审稿时长
14 weeks
期刊介绍: In an ever changing world, plant science is of the utmost importance for securing the future well-being of humankind. Plants provide oxygen, food, feed, fibers, and building materials. In addition, they are a diverse source of industrial and pharmaceutical chemicals. Plants are centrally important to the health of ecosystems, and their understanding is critical for learning how to manage and maintain a sustainable biosphere. Plant science is extremely interdisciplinary, reaching from agricultural science to paleobotany, and molecular physiology to ecology. It uses the latest developments in computer science, optics, molecular biology and genomics to address challenges in model systems, agricultural crops, and ecosystems. Plant science research inquires into the form, function, development, diversity, reproduction, evolution and uses of both higher and lower plants and their interactions with other organisms throughout the biosphere. Frontiers in Plant Science welcomes outstanding contributions in any field of plant science from basic to applied research, from organismal to molecular studies, from single plant analysis to studies of populations and whole ecosystems, and from molecular to biophysical to computational approaches. Frontiers in Plant Science publishes articles on the most outstanding discoveries across a wide research spectrum of Plant Science. The mission of Frontiers in Plant Science is to bring all relevant Plant Science areas together on a single platform.
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