College of Life and Environmental Science, Wenzhou University, Wenzhou, 325035, China.
Zhejiang Provincial Key Laboratory for Water Environment and Marine Biological Resources Protection, Wenzhou University, Wenzhou, 325035, China.
BMC Plant Biol. 2024 Jul 6;24(1):634. doi: 10.1186/s12870-024-05293-0.
Engelhardia (Juglandaceae) is a genus of significant ecological and economic importance, prevalent in the tropics and subtropics of East Asia. Although previous efforts based on multiple molecular markers providing profound insights into species delimitation and phylogeography of Engelhardia, the maternal genome evolution and phylogeny of Engelhardia in Juglandaceae still need to be comprehensively evaluated. In this study, we sequenced plastomes from 14 samples of eight Engelhardia species and the outgroup Rhoiptelea chiliantha, and incorporated published data from 36 Juglandaceae and six outgroup species to test phylogenetic resolution. Moreover, comparative analyses of the plastomes were conducted to investigate the plastomes evolution of Engelhardia and the whole Juglandaceae family.
The 13 Engelhardia plastomes were highly similar in genome size, gene content, and order. They exhibited a typical quadripartite structure, with lengths from 161,069 bp to 162,336 bp. Three mutation hotspot regions (TrnK-rps16, ndhF-rpl32, and ycf1) could be used as effective molecular markers for further phylogenetic analyses and species identification. Insertion and deletion (InDels) may be an important driving factor for the evolution of plastomes in Juglandoideae and Engelhardioideae. A total of ten codons were identified as the optimal codons in Juglandaceae. The mutation pressure mostly contributed to shaping codon usage. Seventy-eight protein-coding genes in Juglandaceae experienced relaxed purifying selection, only rpl22 and psaI genes showed positive selection (Ka/Ks > 1). Phylogenetic results fully supported Engelhardia as a monophyletic group including two sects and the division of Juglandaceae into three subfamilies. The Engelhardia originated in the Late Cretaceous and diversified in the Late Eocene, and Juglandaceae originated in the Early Cretaceous and differentiated in Middle Cretaceous. The phylogeny and divergence times didn't support rapid radiation occurred in the evolution history of Engelhardia.
Our study fully supported the taxonomic treatment of at the section for Engelhardia species and three subfamilies for Juglandaceae and confirmed the power of phylogenetic resolution using plastome sequences. Moreover, our results also laid the foundation for further studying the course, tempo and mode of plastome evolution of Engelhardia and the whole Juglandaceae family.
榉木属（胡桃科）是一个具有重要生态和经济意义的属，普遍存在于东亚的热带和亚热带地区。尽管先前基于多个分子标记的研究为榉木属的物种划分和系统地理学提供了深刻的见解，但榉木属在胡桃科中的母系基因组进化和系统发育仍需要全面评估。在这项研究中，我们对来自 8 个榉木属物种的 14 个样本的质体基因组进行了测序，并结合了来自 36 个胡桃科和 6 个外群物种的已发表数据来测试系统发育分辨率。此外，我们还对质体基因组进行了比较分析，以研究榉木属和整个胡桃科家族的质体基因组进化。
13 个榉木属的质体基因组在基因组大小、基因含量和顺序上高度相似。它们表现出典型的四分体结构，长度在 161069bp 到 162336bp 之间。三个突变热点区域（TrnK-rps16、ndhF-rpl32 和 ycf1）可作为进一步系统发育分析和物种鉴定的有效分子标记。插入和缺失（InDels）可能是 Juglandoideae 和 Engelhardioideae 质体进化的重要驱动因素。总共鉴定出 10 个密码子为胡桃科的最佳密码子。突变压力主要导致密码子使用的形成。在胡桃科中，有 78 个蛋白质编码基因经历了松弛的纯化选择，只有 rpl22 和 psaI 基因表现出正选择（Ka/Ks>1）。系统发育结果充分支持榉木属是一个单系群，包括两个节和将胡桃科分为三个亚科。榉木属起源于晚白垩世，在始新世晚期多样化，而胡桃科起源于早白垩世，在中白垩世分化。系统发育和分歧时间不支持榉木属在进化历史中发生快速辐射。
我们的研究充分支持了对榉木属物种的节和胡桃科的三个亚科的分类处理，并证实了使用质体序列进行系统发育分辨率的有效性。此外，我们的研究结果还为进一步研究榉木属和整个胡桃科家族的质体进化过程、速度和模式奠定了基础。
