State Key Laboratory of Plant Diversity and Specialty Crops & Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences (IBCAS), Beijing, 100093, China.
BMC Plant Biol. 2024 Oct 21;24(1):989. doi: 10.1186/s12870-024-05702-4.
Evidence shows that full mycoheterotrophs and holoparasites often have reduced plastid genomes with rampant gene loss, elevated substitution rates, and deeply altered to conventional evolution in mitochondrial genomes, but mechanisms of cytonuclear evolution is unknown. Endoparasitic Sapria himalayana and mycoheterotrophic Gastrodia and Platanthera guangdongensis represent different heterotrophic types, providing a basis to illustrate cytonuclear evolution. Here, we focused on nuclear-encoded plastid / mitochondrial (N-pt / mt) -targeting protein complexes, including caseinolytic protease (ClpP), ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo), oxidative phosphorylation system (OXPHOS), DNA recombination, replication, and repair (DNA-RRR) system, and pentatricopeptide repeat (PPR) proteins, to identify evolutionary drivers for cytonuclear interaction.
The severity of gene loss of N-pt PPR and pt-RRR genes was positively associated with increased degree of heterotrophy in full mycoheterotrophs and S. himalayana, while N-mt PPR and mt-RRR genes were retained. Substitution rates of organellar and nuclear genes encoding N-pt/mt subunits in protein complexes were evaluated, cytonuclear coevolution was identified in S. himalayana, whereas disproportionate rates of evolution were observed in the OXPHOS complex in full mycoheterotrophs, only slight accelerations in substitution rates were identified in N-mt genes of full mycoheterotrophs.
Nuclear compensatory evolution was identified in protein complexes encoded by plastid and N-pt genes. Selection shaping codon preferences, functional constraint, mt-RRR gene regulation, and post-transcriptional regulation of PPR genes all facilitate mito-nuclear evolution. Our study enriches our understanding of genomic coevolution scenarios in fully heterotrophic plants.
有证据表明，完全菌根异养植物和全寄生植物的质体基因组往往会发生严重的基因丢失，取代率升高，线粒体基因组的进化方向也与传统进化大相径庭，但细胞-核进化的机制尚不清楚。内寄生的 Sapria himalayana 和菌根异养 Gastrodia 和 Platanthera guangdongensis 代表了不同的异养类型，为阐明细胞-核进化提供了基础。在这里，我们重点研究了核编码质体/线粒体（N-pt / mt）靶向蛋白复合物，包括蛋白酶体（ClpP）、核酮糖-1,5-二磷酸羧化酶/加氧酶（RuBisCo）、氧化磷酸化系统（OXPHOS）、DNA 重组、复制和修复（DNA-RRR）系统以及五肽重复（PPR）蛋白，以确定细胞-核相互作用的进化驱动因素。
N-pt PPR 和 pt-RRR 基因的基因丢失严重程度与完全菌根异养植物和 S. himalayana 的异养程度呈正相关，而 N-mt PPR 和 mt-RRR 基因得以保留。评估了编码蛋白复合物中细胞器和核基因的 N-pt/mt 亚基的取代率，鉴定出 S. himalayana 中的细胞-核协同进化，而在完全菌根异养植物中观察到 OXPHOS 复合物的进化不成比例，仅在完全菌根异养植物的 N-mt 基因中鉴定到轻微的取代率加速。
在质体和 N-pt 基因编码的蛋白复合物中鉴定到核的补偿进化。选择塑造密码子偏好、功能约束、mt-RRR 基因调控以及 PPR 基因的转录后调控都促进了线粒体-核的进化。我们的研究丰富了对完全异养植物中基因组协同进化的认识。
