Chloroplast Genome Evolution, Heteroplasmy, and Inverted Repeat Dynamics in the Elymus Complex (Triticeae, Poaceae): Insights from Single-Molecule Sequencing of Elymus ciliaris and Comparative Analysis of St-Genome Lineages.

IF 4.1 2区生物学 Q1 PLANT SCIENCES

Annals of botany Pub Date : 2026-10-14 DOI:10.1093/aob/mcag333

Negar Karimi, Yangmeng Zhang, Hojjatollah Saeidi, Trude Schwarzacher, Qing Liu, J S Pat Heslop-Harrison

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引用次数: 0

Abstract

Background/objectives: Elymus sensu lato (Poaceae) is arguably the largest and most complex genus in the tribe Triticeae. It includes hybrids and polyploids based on x=7 chromosomes, all including the St genome, forming a valuable genepool for forage grass and cereal breeding. Analysis of chloroplast genome diversity and structural dynamics is critical for resolving maternal lineages, reticulate evolution and biodiversity across this agronomically important complex, refining their taxonomy, conservation and exploitation.

Methods: We sequenced the complete chloroplast genome (plastome) of Elymus ciliaris (4x=2n=28; StStYY) using ultra-long Oxford Nanopore single-molecule reads and compared it to 77 additional chloroplast genomes representing major St-genome lineages in Elymus s.l. (Pseudoroegneria St; Elymus s.s. StH, StY; Thinopyrum StJ/E; Campeiostachys StYH; Kengyilia StYP). We analyzed structure, nucleotide diversity, inverted repeat (IR) dynamics, and phylogenetic signal.

Results: The E. ciliaris chloroplast genome was 135,008 bp long (38.3% GC) with a canonical quadripartite structure. Single-molecule reads (n=81) revealed heteroplasmy: two Small-Single-Copy (SSC) orientations at 30%:70% frequency, indicating an inversion polymorphism. Across the Elymus group, comparative analysis of chloroplast assemblies showed high structural conservation but lineage-specific IR-boundary shifts. Kengyilia exhibits exceptional IR expansion. Nucleotide diversity hotspots localize to the large single-copy region, especially in StY lineages. Phylogenies recover a monophyletic St-containing clade but do not delineate genera, reflecting reticulate evolution.

Conclusions: Single-molecule sequencing uncovered heteroplasmy with an inversion polymorphism in a single plant of Elymus ciliaris, hidden in short read assemblies. There were no other polymorphisms, as expected for chloroplast sequences. Our analyses showed that a Pseudoroegneria-like St chloroplast genome predominates as the maternal donor across Elymus polyploids. Variable regions and IR dynamics offer strong models for chloroplast genome evolution in reticulate lineages and suggest exploiting plastome variation to complement nuclear biodiversity studies.

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小麦科麦草群中叶绿体基因组进化、异质性和反向重复动力学：来自毛毛麦草单分子测序和St-Genome谱系比较分析的见解。

背景/目的：羊草属（禾本科）是小麦科中最大、最复杂的属。它包括基于x=7染色体的杂交种和多倍体，都包括St基因组，形成了一个有价值的饲草和谷物育种基因库。叶绿体基因组多样性和结构动力学分析是解决母系谱系、网状进化和生物多样性，完善其分类、保护和利用的关键。方法：利用超长Oxford Nanopore单分子测序技术对毛毛榆（Elymus ciliaris）（4x=2n=28; StStYY）的叶绿体基因组（质体组）进行测序，并与其他77个代表主要St基因组谱系的叶绿体基因组（Pseudoroegneria St; Elymus s.s.s . StH, StY; Thinopyrum StJ/E; Campeiostachys StYH; Kengyilia StYP）进行比较。我们分析了其结构、核苷酸多样性、反向重复序列（IR）动力学和系统发育信号。结果：纤毛虫叶绿体基因组长135,008 bp (38.3% GC)，具有典型的四分体结构。单分子reads （n=81）显示异质性：两个Small-Single-Copy （SSC）取向在30%:70%的频率，表明反转多态性。在整个羊草类群中，叶绿体组装的比较分析显示出高度的结构保守性，但谱系特异性的ir边界偏移。肯吉利亚表现出异常的红外扩张。核苷酸多样性热点集中在大的单拷贝区域，特别是在StY谱系中。系统发育恢复一个单系的含st的进化枝，但不描述属，反映网状进化。结论：单分子测序揭示了单株羊草（Elymus ciliaris）中隐藏在短读片段中的异质倒置多态性。没有其他多态性，正如预期的叶绿体序列。我们的分析表明，一个类似假卵细胞的St叶绿体基因组作为母系供体在羊草多倍体中占主导地位。可变区域和红外动态为网状谱系的叶绿体基因组进化提供了强有力的模型，并建议利用质体变异来补充核生物多样性的研究。

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来源期刊

Annals of botany 生物-植物科学

CiteScore

7.90

自引率

4.80%

发文量

138

审稿时长

3 months

期刊介绍： Annals of Botany is an international plant science journal publishing novel and rigorous research in all areas of plant science. It is published monthly in both electronic and printed forms with at least two extra issues each year that focus on a particular theme in plant biology. The Journal is managed by the Annals of Botany Company, a not-for-profit educational charity established to promote plant science worldwide. The Journal publishes original research papers, invited and submitted review articles, ''Research in Context'' expanding on original work, ''Botanical Briefings'' as short overviews of important topics, and ''Viewpoints'' giving opinions. All papers in each issue are summarized briefly in Content Snapshots , there are topical news items in the Plant Cuttings section and Book Reviews . A rigorous review process ensures that readers are exposed to genuine and novel advances across a wide spectrum of botanical knowledge. All papers aim to advance knowledge and make a difference to our understanding of plant science.