Comparative genomics of orobanchaceous species with different parasitic lifestyles reveals the origin and stepwise evolution of plant parasitism

Abstract

Orobanchaceae is the largest family of plant parasites comprising autotrophic and parasitic plants with all degrees of parasitism, making it by far the best family for studying the origin and evolution of plant parasitism. Here we provide three high-quality genomes of orobanchaceous plants, the autotrophic Lindenbergia luchunensis and holoparasitic Phelipanche aegyptiaca and Orobanche cumana. Phylogenomic analysis on these three genomes and the previously published genomes and transcriptomes of other orobanchaceous species created a robust phylogenetic framework of Orobanchaceae. An ancient whole-genome duplication (WGD; about 79.29 Mya) was detected in the common ancestor of Orobanchaceae and Mimulus guttatus, and this event might have contributed to the origin of parasitism; however, except for Striga, no WGD events occurred in any lineages of orobanchaceous parasites after divergence from their autotrophic common ancestor, and the expansion of the genomes of orobanchaceous parasitic plants was mainly due to retrotransposons. We detected evident convergent gene loss in all parasites within Orobanchaceae and between Orobanchaceae and dodder Cuscuta australis. The gene families in the orobanchaceous parasites showed a clear pattern of recent gains and expansions, and the expanded gene families are enriched in functions related to development of haustorium. Thus, recent gene family expansions may have facilitated the adaptation of orobanchaceous parasites to different hosts. These data well support the previously proposed model of parasitic plant genome evolution. This work illustrates the trajectory of the evolution of orobanchaceous parasites, and will facilitate future studies on parasitism and the control of parasitic plants in agriculture.

Rethinking convergence in plant parasitism integrating molecular and population genetic processes

“…Recent genomic studies enabled comprehensive surveys of the gene repertoire in Cuscuta, Orobanchaceae, and Rafflesiaceae. They consistently reported significant gene losses in photosynthesis related functions including plastid organization and pigment metabolism, which aligns well with the prediction of the funnel model (Vogel et al, 2018;Cai et al, 2021;Xu et al, 2022;Chen et al, 2022). Meanwhile, unexpected gene losses were found in the biosynthesis of abscisic acid (ABA) in Sapria (Rafflesiaceae; Cai et al, 2021).…”

“…In addition to Cuscuta, a very similar pattern of flowering synchronization is observed in the lesser broomrape Orobanche minor (Holdsworth and Nutman, 1947). As more genomic resources become available in Orobanchaceae (Xu et al, 2022), comparative genomic tools can be used to identify the pathways modulating life-cycle events in Orobanche and test whether their evolution follows a similar coordinated manner as in Cuscuta.…”

“…In parasitic plants, the most well-known example comes from the strigolactone receptor gene KAI2d in Orobanchaceae, which proliferated in the genome via tandem and genome duplication and contributed to host range expansion (Conn et al, 2015;Yoshida et al, 2019). A recent comprehensive survey across six Orobanchaceae genomes reported that 11% of the highly expressed genes in the haustoria originated from a shared genome duplication event in the common ancestor of Orobanchaceae and Mimulus (Xu et al, 2022). In Sapria, however, GO analysis on expanded gene families only identified broad categories including chromosome organization, DNA metabolism, and cell cycle (Cai et al, 2021), suggesting that the creation and retention of duplicated genes are likely to be a lineage specific process.…”

“…In Cuscuta, LTR and satellite DNA drove a 102-fold variation in genome sizes within 23 Myr (Neumann et al, 2021). In both Sapria and Phelipanche (Orobanchaceae), TEs account for ~90% of the total genome sizes (Cai et al, 2021;Neumann et al, 2021;Xu et al, 2022). Besides being a constant threat to genome integrity, TEs also generate adaptive phenotypes in the face of stressful conditions (Capy et al, 2000;Kazazian Jr, 2004).…”