A high-quality genome provides insights into the new taxonomic status and genomic characteristics of Cladopus chinensis (Podostemaceae)

Ting Xue,Wan Cen,Binghua Chen,Wenfang Fan,Youqiang Chen,Jinmao Zhu,Jiannan Chen,Xingtan Zhang,Limin Liang,Duo Chen,Zhen Huang,Shuai Chen,Nan Chen,Xuehai Zheng

doi:10.1038/s41438-020-0269-5

Ting Xue, Wan Cen + Show 12 more

Open Access

https://doi.org/10.1038/s41438-020-0269-5

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Abstract

The Podostemaceae are ecologically and morphologically unusual aquatic angiosperms that survive only in rivers with pristine hydrology and high water quality and are at a relatively high risk of extinction. The taxonomic status of Podostemaceae has always been controversial. Here, we report the first high-quality genome assembly for Cladopus chinensis of Podostemaceae, obtained by incorporating Hi-C, Illumina and PacBio sequencing. We generated an 827.92 Mb genome with a contig N50 of 1.42 Mb and 27,370 annotated protein-coding genes. The assembled genome size was close to the estimated size, and 659.42 Mb of the assembly was assigned to 29 superscaffolds (scaffold N50 21.22 Mb). A total of 59.20% repetitive sequences were identified, among which long terminal repeats (LTRs) were the most abundant class (28.97% of the genome). Genome evolution analysis suggested that the divergence time of Cladopus chinensis (106 Mya) was earlier than that of Malpighiales (82 Mya) and that this taxon diverged into an independent branch of Podestemales. A recent whole-genome duplication (WGD) event occurred 4.43 million years ago. Comparative genomic analysis revealed that the expansion and contraction of oxidative phosphorylation, photosynthesis and isoflavonoid metabolism genes in Cladopus chinensis are probably related to the genomic characteristics of this growing submerged species. Transcriptome analysis revealed that upregulated genes in the shoot group compared to the root group were enriched in the NAC gene family and transcription factors associated with shoot development and defense responses, including WUSCHEL (WUS), ASYMMETRIC LEAVES (ASL), SHOOT MERISTEMLESS (STM), NAC2, NAC8, NAC29, NAC47, NAC73, NAC83 and NAC102. These findings provide new insights into the genomic diversity of unusual aquatic angiosperms and serve as a valuable reference for the taxonomic status and unusual shoot apical meristem of Podostemaceae.

Highlights

Podostemaceae are freshwater hydrophytes whose center of diversity is the Neotropics
When we sought to investigate the environmental adaptation of C. chinensis, we found that a series of photosynthesis and energy metabolism-associated gene families exhibit significant expansion, including the NADPH oxidase (NDHF, NDHB1, GPSA), NADH dehydrogenase (NAD1, NDHD, NAD4L, NAD7, NDHG), chlorophyll a-b binding protein (LHCB) and cytochrome P450 (CYP86) families (Table S13)
To identify the potential key genes or transcription factors involved in shoot formation in C. chinensis, we identified 609 genes that were highly expressed in shoots (Table S22; Fig. S10), and these highly expressed genes were significantly enriched in the metabolic process, stimulus response, developmental process, environmental adaptation, signal transduction, energy metabolism, carbohydrate metabolism and secondary metabolite synthesis were identified according to Kyoto Encyclopedia of Genes and Genomes (KEGG) and Gene Ontology (GO) enrichment analyses

Summary

Introduction

Podostemaceae are freshwater hydrophytes whose center of diversity is the Neotropics. The Amazon is the richest region of Podostemaceae occurrence[2]. These plants require rivers with pristine hydrology and good water quality, which are very important characteristics for their productivity and for maintaining the associated fauna, and their destruction can lead to ecological and economic losses as well as the loss of cultural and hedonic value[3,4]. Angiosperms normally exhibit a common system of gravitropism (the growth movement of organs in response to gravity). The roots grow downward into the soil, and the shoots upward in this gravitropism system. The plant meristems, including the root apical meristem (RAM) and shoot apical meristem (SAM), are unique structures of undifferentiated pluripotent stem cells[7]. Podostemaceae, Streptocarpus and Lemnaceae exhibit unusual modifications of the SAM that may reflect adaptation to new habitats and can subsequently diversify in the evolution of plants[8]

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