Progress has been made in the study of the ancestral genome evolution of calamus and monocotyledonous plants

On July 14, 2022, Nature Plants published important results from The Wuhan Botanical Garden of the Chinese Academy of Sciences Wang Qingfeng, Chen Jinming’s team and French collaborators, announcing the genome of Acorus tatarinowii, an important aquatic medicinal plant in calamus, the earliest branch of monocotyledonous plants, and the relevant research preliminarily revealed the early genome evolution process and law of the ancestors of monocotyledonous plants. It lays an important foundation for understanding the radiation evolution process of monocotyledonous plants, including grasses.

Monocotyledonous plants are one of the important branches of flowering plants (angiosperms), accounting for about 21% of the species diversity of angiosperms, including important horticultural crops such as bananas, asparagus, coconuts and bulk food crops such as rice, wheat and corn. According to the taxonomy and molecular phylogeny of large-scale sampling, Acorales is the earliest extant branching taxon of monocotyledonous plants, which is a sister group with all other monocotyledonous plants, similar to the phylogenous status of the oilless camphor of the early branches of angiosperms and the early branches of true dicotyledonous plants, and the calamus species are important materials for exploring and revealing the early evolution of monocotyledonous plants.

Monocotyledonous plants are clearly different from other flowering plants in terms of morphological characteristics (such as roots, leaf veins, etc.), and the early origin of their ancestors is one of the hot issues of plant evolutionary biology, and the earliest fossil records of monocotyledonous plants can be traced back to the early Cretaceous period. In addition to the fact that the basal monocotyledonous plants (calamus, Zephyllaceae, Hydroptera, etc.) are mostly aquatic and hygrological plants, the fossil records of early aquatic monocotyledonous plants (such as Zephyllaceae, etc.) appear at least in the Upper Cretaceous Period, and some scholars have proposed that the ancestors of monocotyledonous plants originated in the aquatic environment, but the speculation of the aquatic origin of the ancestors of monocotyledonous plants still needs more evidence of paleontology and genomic evolution. Comparative analysis of the linear sequencing changes in genes or homologous fragments in the genomes of sequenced monocotyledonous plant species will help to understand the key influencing factors driving the evolutionary trajectory of monocotyledonous plants. In the process of radiation differentiation of monocotyledonous plants, the phenomenon of whole genome duplication or paleoploidy (WGD) is very common, which is considered to be one of the key mechanisms to promote species diversification and adaptation to the environment, and how paleoseploidy and its derived genome rearrangement promote the diversification of monocotyledonous plants needs to be solved urgently.

In response to the above scientific problems, the Wuhan Botanical Garden, in cooperation with the French National Institute of Agri-Food and Environment, used PacBio and Hi-C technology to complete the sequencing of the whole genome of calamus and the assembly at the chromosome level. Genome-wide comparative analysis with other monocotyledonous plants found that calamus had experienced only one independent paleoploidy event accompanied by subgenome dominance, and that genome doubling occurred 2 or more times in other monocotyledonous plants except calamus and marine plant macrophyllum macrophyllum (Figure 1). Among the monocotyledonous plants involved in the study, the genomic structure evolution of calamus calamus (linear ordering/collinearity of genes on chromosomes) and amino acid sequence replacement rates were the most slow and conserved. Further correlation analysis also found that the relative conservatism of the collinear structure of the genomes of each species was significantly correlated with their sequence replacement rate and the number of genome doublings, which may be the reason for the relatively slow evolution of the genome structure of calamus calamus. The comparative analysis of the genome structure of representative monocotyledonous plants with the outer taxa (lotus) shows that the degree of methylation in the upstream and downstream regions of genes and the tissue specificity of gene expression may be important factors restricting the evolution of genome structure.

Fig. 1 Collinear comparison of monocotyledonous plant ancestral karyotype (AMK) and early clade monocotyledonous plants with whole genome replication (Ata: Calamus lithophyllum)

Based on calamus and other early branch species of monocotyledonous plants, the study updated the previously constructed pre-τ-τ period monocotyledonous plant ancestor karyotype (pre-τ AMK, 2n = 10) (Murat et al., 2017, Nature Genetics, doi: 10.1038/ng.3813) to the 12 chromosomes (AMK, 2n = 12) of the earliest ancestors of monocotyledonous plants (Figure 2). Based on this ancestral karyotype, the early karyotype evolution of monocotyledonous plants is repeated: the karyotype of calamus is formed by the ancestor of the monocotyledonous plant AMB (n = 6) through its unique genome doubling to form n = 12 chromosome intermediates, followed by 12 chromosome fusions to form its current 12 modern chromosomes (Figure 3). The study also found that grasses (such as rice) have historically experienced more chromosome rearrangement events such as fusion and division than taxa of earlier branches such as calamus.

Fig. 2 Construction of ancestral chromosomes of monocotyledonous plants and their early karyotype evolution

Figure 3 Evolution from the ancestral chromosomes of monocotyledonous plants to the karyotype of the chromosomes of calamus calamus

In terms of gene family evolution, the study reveals important functional gene family evolution events associated with early morphological evolution of monocotyledonous plants and adaptation to wetlands or aquatic habitats such as degradation of parallel leaf veins and primary roots, and low levels of inorganic phosphate aquatic environments. For example, in Arabidopsis, the DOT3 (DEFECTIVELY ORGANIZED TRIBUTARIES 3) gene has been shown to cause defects in seedling and primary root growth and produce abnormal parallel veining in young leaves, dot3 has been lost in both monocotyledonous plants and aquatic water lilies (water lily, mustard), possibly associated with specific traits such as parallel/palmar leaf veins and primary root (taproot) degradation in both taxa (Figure 4).

Fig. 4 The DOT3 gene that affects the development of leaf veins and taperomes in Arabidopsis thaliana is lost simultaneously in monocotyledonous plants and water lily plants

The research results were published in Nature Plants under the title “The slow-evolving Acorus tatarinowii genome sheds light on ancestral monocot evolution.” Shi Tao, Associate Researcher of key laboratory of Aquatic Plants and Watershed Ecology of Chinese Academy of Sciences/Wuhan Botanical Garden, is the first author, Professor Jerome Salse of the French National Institute of Agri-Food and Environment, And Researcher Chen Jinming and Researcher Wang Qingfeng of Wuhan Botanical Garden are co-corresponding authors. The relevant research work has been funded by the Strategic Pilot Science and Technology Project of the Chinese Academy of Sciences (XDB31000000), the National Natural Science Foundation of China (32170240, 31570220 and 31870208), and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (2019335). (Source: Wuhan Botanical Garden, Chinese Academy of Sciences)

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