Discussion
Vitaceae is a sister to most of the Rosids in the highly diverse Rosid clade of the flowering plants (Soltis et al., 2000). Grape (V. vinifera ) was believed as one of the most slowly evolved species representing a more conserved ancestral structure of the genome that can be used to unravel the evolution and genome duplication history of other eudicots (Murat et al., 2017). Here, we present another genome in Vitaceae, C. rotundifolia , to show probable diverse evolutionary history considering distinct ecological niches. It is exciting to observe the evidence of the palaeo-hexaploidy event shared byCissus and grape. Moreover, the lack of any other WGDs suggestsCissus also might hold a relatively ancestral state of genome organization after divergence from their common ancestors (Chanderbali et al., 2022; Qin et al., 2021; Van de Peer et al., 2009). This would be reflected by ~13.7 % of the total genes inCissus (~17.7 % of grape) belonging to the 3:1 duplicated region to Amborella and considerable high collinearity of chromosomes to grape. Besides, we proposed that more frequent chromosome shuffling, including at least five independent fusion events, might occur in Cissus after its origin (three fusions in grape). The recent segmental duplications probably further accounted for the increased genetic and biological complexity (Bondino et al., 2012), together with chromosome fusions serving as a prelude to the modern karyotype configuration of Vitaceae.
The very recent burst of activity in LTRs (90.77 kya) detected inCissus could probably be explained by the severe climate transition from arid to wet that occurred in the past 100 kya in eastern Africa, where substantial ecological habitats turnover was recorded (Figure 1d) (Alzohairy et al., 2012). However, such server invasion of retrotransposons left a smaller genome (350.69 Mb) than grape (475 Mb). Indeed, we found much higher gene density in Cissus than in grape, indicating the lower frequency of repeats in intergenic regions where LTR insertion is usually preferred (Table S32). Moreover,Cissus probably had experienced a fair loss of ancient genomic arrays compared to grape. Together, transposable element removal and sequence elimination accompanied by chromosomal rearrangement (e.g., chromosomal fusion and recombination) could contribute to the selected, size-reduced genome of Cissus (Wan et al., 2021; Xiong et al., 2011). Nevertheless, a small genome size could be particularly advantageous for plants to enhance water use efficiency through increased stomatal responsiveness of smaller cells (Drake et al., 2013; Roddy et al., 2020).
Seasonal drought is one of the biggest challenges for agriculture in East Africa. The evolution of the water storage tissue of plants is the most common adaptive strategy in arid and semi-arid regions (Eggli and Nyffeler, 2009). The leaves of C. rotundifolia are succulent, which exemplifies a convergent evolution with plants from dry habitats like Agave (Newton & Chan, 1998). We found gene families of enzymes responsible for the polysaccharide synthesis, such as pectate lyase and pectinesterase, were remarkably expanded in Cissus . Therefore, modified pectin and other polysaccharides in cells may confer to the occurrence of succulent leaves (Morse, 1990). Signature of the noticeable proliferation of gene families associated with biotic and abiotic responses (i.e., P450 , LEA , and LRR ) would play key roles in the objective arms race against pathogens and unfavorable environment (Hundertmark and Hincha, 2008; Plomion et al. , 2018; Rai et al., 2015).
A clear pattern of selective amplification of immunity genes inCissus and Vitis was present, indicating a potential functional divergence related to adaptations. Further, succulent-specific expansion in a certain gene family (e.g.,terpene synthase ’, ‘HSP20-like ’) suggested a convergent mechanism in such a morphologically modified group. Interestingly, the succulent fashion of TD retention was also correlated to morphological innovation, which might unveil another functional bias pattern of TD content in the face of rapid and intense environmental change during seed plant evolution.
The innovation of the CAM photosynthetic pathway in Cissusfurther contributes to its adaptation in the dry savannas by enhancing the WUE (Bloom and Troughton, 1979). The decarboxylation inCissus is likely induced in two ways: one is driven by ME and PPDK enzymes, and another is catalyzed by PEPCK enzyme (Figure 4c, Figure S8). For decarboxylase process, ME and PPDK enzymes were used inK. fedtschenkoi and PEPCK enzyme was utilized in pineapple (Ming et al., 2015; Yang et al., 2017). The genes had undergone convergent evolution in Kalanchoë fedtschenkoi , which included PEPC, nucleosome assembly protein 1-like 4 (NAP1L4), transcription factor hy5-like protein (HY5), and chloroplast-localized glucose-6-phosphate isomerase (GPI). However, no amino acids showed convergent evolution patterns for CAM and stoma-related genes in Cissus by a similar analysis (Yang et al., 2017), suggesting that the evolution of the characteristics may be derived from multiple modifications. InSedum album , the number variation of cis -elements between C3 and CAM-cycling status showed a phase shift during the daytime (Wai et al., 2019). While cis -elements of CAM cycling genes inIsoetes howellii are not strongly associated with transcript expression, additionally lacking ME and G-box on promoters of CAM genes (Wickell et al., 2021). The EE is over-presented in the promoter of evening-phased genes (Huang et al., 2016). Compared to other plants (Ming et al., 2015), βCA1 with one EE in Cissus maybe contribute to CO2 fixation during nighttime (Table S30). The identification of cis -regulatory elements in the promoter of CAM genes in C. rotundifolia would help to explain the evolution of CAM from C3 plants and provide valuable information for breeding drought-tolerant crops.