Large-scale gene losses underlie the genome evolution of parasitic plant <i>Cuscuta australis</i>

Sun, Guiling; Xu, Yuxing; Liu, Hui; Sun, Taixiang; Zhang, Jingxiong; Hettenhausen, Christian; Shen, Gary X.; Qi, Jinfeng; Qin, Yan; Li, Jing; Wang, Lei; Chang, Wei; Guo, Zhenhua; Baldwin, Ian T.; Wu, Jianqiang

doi:10.1101/285593

Cited by 36 publications

(75 citation statements)

References 60 publications

(65 reference statements)

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“…Low BUSCO scores have also been noted in other plants with morphological innovations like the parasitic dodder plant (Cuscuta) and carnivorous bladderwort (Utricularia) that both also lack roots and leaf structures like Wolffia (Ibarra-Laclette et al 2013;Sun et al 2018;Vogel et al 2018). Cuscuta australis shares many of the same gene losses as Wolffia such as WOX5 (root apical stem cell maintenance), LOP1 (leaf patterning and root development) and the entire family of casparian strip genes (CASP) (Sun et al 2018). Wolffia is also missing several families of the small signaling peptide CLAVATA3/ESR-RELATED (CLE) that regulate various aspects of cell fate and meristem size (Jun et al 2010).…”

Section: Discussionmentioning

confidence: 94%

“…Multiple independently assembled genomes of both Spirodela and Wolffia share a common set of missing BUSCO genes ( Figure S6), and many of these genes in Wolffia represent genes associated with its morphological innovations ( Figure 2; Table S5). Low BUSCO scores have also been noted in other plants with morphological innovations like the parasitic dodder plant (Cuscuta) and carnivorous bladderwort (Utricularia) that both also lack roots and leaf structures like Wolffia (Ibarra-Laclette et al 2013;Sun et al 2018;Vogel et al 2018). Cuscuta australis shares many of the same gene losses as Wolffia such as WOX5 (root apical stem cell maintenance), LOP1 (leaf patterning and root development) and the entire family of casparian strip genes (CASP) (Sun et al 2018).…”

Section: Discussionmentioning

confidence: 99%

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Genome and time-of-day transcriptome ofWolffia australianalink morphological extreme minimization with un-gated plant growth

Michael

Ernst

Hartwick

et al. 2020

Preprint

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Wolffia is the fastest growing plant genus on Earth with a recorded doubling time of less than a day. Wolffia has a dramatically reduced body plan, primarily growing through a continuous, budding-type asexual reproduction with no obvious phase transition. Most plants are bound by the 24-hour light-dark cycle with the majority of processes such as gene expression partitioned or phased to a specific time-of-day (TOD). However, the role that TOD information and the circadian clock plays in facilitating the growth of a fast-growing plant is unknown. Here we generated draft reference genomes for Wolffia australiana (Benth.) Hartog & Plas to monitor gene expression over a two-day time course under light-dark cycles. Wolffia australiana has the smallest genome size in the genus at 357 Mb and has a dramatically reduced gene set at 15,312 with a specific loss of root (WOX5), vascular (CASP), circadian (TOC1), and light-signaling (NPH3) genes. Remarkably, it has also lost all but one of the NLR genes that are known to be involved in innate immunity. In addition, only 13% of its genes cycle, which is far less than in other plants, with an overrepresentation of genes associated with carbon processing and chloroplast-related functions. Despite having a focused set of cycling genes, TOD cis-elements are conserved in W. australiana, consistent with the overall conservation of transcriptional networks. In contrast to the model plants Arabidopsis thaliana and Oryza sativa, the reduction in cycling genes correlates with fewer pathways under TOD control in Wolffia, which could reflect a release of functional gating. Since TOD networks and the circadian clock work to gate activities to specific times of day, this minimization of regulation may enable Wolffia to grow continuously with optimal economy. Wolffia is an ideal model to study the transcriptional control of growth and the findings presented here could serve as a template for plant improvement.

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Section: Discussionmentioning

confidence: 94%

Section: Discussionmentioning

confidence: 99%

Genome and time-of-day transcriptome ofWolffia australianalink morphological extreme minimization with un-gated plant growth

Michael

Ernst

Hartwick

et al. 2020

Preprint

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“…One prerequisite for achieving a better understanding of the molecular processes and mechanisms of a Cuscuta attack is a reference genome. Recently, complete genome sequences have been published for two Cuscuta species, C. campestris and C. australis (Sun et al, 2018; Vogel et al, 2018). However, two significant bottlenecks to perform targeted genome manipulations remain in the form of low transformation efficiency and poor regeneration rates of Cuscuta tissues in vitro .…”

Section: Introductionmentioning

confidence: 99%

“…What has made these hairy roots popular for plant biotechnology is that they can be propagated in the absence of exogenous plant hormones. Very recently, it was shown that an A. rhizogenes gene coding for the mikimopine synthase was horizontally transferred into several Cuscuta species (Zhang et al, 2020), including Cuscuta campestris (Vogel et al, 2018) and Cuscuta australis (Sun et al, 2018), suggesting that Cuscuta species may be susceptible to infection by this Agrobacterium species despite their lack of roots.…”

Section: Introductionmentioning

confidence: 99%

A highly efficient protocol for transformingCuscuta reflexabased on artificially induced infection sites

Lachner

Galstyan

Krause

2020

Preprint

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A protocol that yields high numbers of transformed cells in the adhesive disks of Cuscuta reflexa 27 upon exposure to agrobacteria brings closer the vision of generating genetically modified 28 Cuscuta. 29 30 ABSTRACT 31 A current bottleneck in the functional analysis of the emerging parasitic model plant Cuscuta and 32 the exploitation of its recently sequenced genomes is the lack of efficient transformation tools. 33 Here, we describe the development of a novel highly efficient Agrobacterium-mediated 34 transformation protocol for Cuscuta reflexa based on the parasitic structure referred to as 35 adhesive disk. Both, Agrobacterium rhizogenes and Agrobacterium tumefaciens carrying binary 36 transformation vectors with reporter fluorochromes yielded high numbers of transformation 37 events. An overwhelming majority of transformed cells were observed in the cell layer below the 38 adhesive disk's epidermis, suggesting that these cells are particularly susceptible to infection. Co-39 transformation of these cells happens frequently when Agrobacterium strains carrying different 40 constructs are applied together. Explants containing transformed tissue expressed the fluorescent 41 markers in in vitro culture for several weeks, offering a possibility for development of 42 transformed cells into callus. 43 44 45 3 46 48 worldwide and infects a broad range of host plants. The parasite starts an attack by winding 49around the host stem. A multicellular feeding structure termed the haustorium, which can reach 50 2-3 mm in size in some species and originates from a secondary meristem in the cortex close to 51 the vascular bundles, develops within a few days and breaches the host tissue integrity using 52 mechanical pressure and enzymatic digestion of cell walls (Nagar et al., 1984; Johnsen et al., 53 2015; Kaiser et al., 2015). To make the penetration possible, a sucker-shaped attachment organ 54 provides the necessary counterforce. The development of this organ, termed "adhesive disk" or 55

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“…Despite many studies aimed at analyzing the transcriptional changes that occur during haustorium development and host infection in various species of parasitic plants (Ranjan et al ., 2014; Yang et al ., 2015; Zhang et al, 2015; Ichihashi et al ., 2015, Sun et al ., 2018; Yoshida et al ., 2019), there have been few functional studies of these haustorium-specific genes. To explore the molecular mechanisms of parasitism, including haustorium organogenesis, we established a model parasitic plant system using Phtheirospermum japonicum , a facultative parasitic plant in the Orobanchaceae (Ishida et al ., 2016; Spallek et al ., 2017).…”

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confidence: 99%

Subtilase activity in the intrusive cells mediates haustorium maturation in parasitic plants

Ogawa

Wakatake

Spallek

et al. 2020

Preprint

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Parasitic plants that infect crops are devastating to agriculture throughout the world. They develop a unique inducible organ called the haustorium, which connects the vascular systems of the parasite and host to establish a flow of water and nutrients. Upon contact with the host, the haustorial epidermal cells at the interface with the host differentiate into specific cells called intrusive cells that grow endophytically towards the host vasculature. Then, some of the intrusive cells re-differentiate to form a xylem bridge that connects the vasculatures of the parasite and host. Despite the prominent role of intrusive cells in host infection, the molecular mechanisms mediating parasitism in the intrusive cells are unknown. In this study, we investigated differential gene expression in the intrusive cells of the facultative parasite Phtheirospermum japonicum in the family Orobanchaceae by RNA-Sequencing of laser-microdissected haustoria. We then used promoter analyses to identify genes that are specifically induced in intrusive cells, and used promoter fusions with genes encoding fluorescent proteins to develop intrusive cell-specific markers. Four of the intrusive cell-specific genes encode subtilisin-like serine proteases (SBTs), whose biological functions in parasitic plants are unknown. Expression of an SBT inhibitor in the intrusive cells inhibited their development, inhibited the development of the xylem bridge, and reduced auxin response levels near the site where the xylem bridge normally develops. Therefore, we propose that subtilase activity plays an important role in haustorium development in this parasitic plant.One sentence summaryTissue-specific analysis showed that the subtilases specifically expressed in intrusive cells regulate auxin-mediated host-parasite connections in the parasitic plant Phtheirospermum japonicum.

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Large-scale gene losses underlie the genome evolution of parasitic plant Cuscuta australis

Cited by 36 publications

References 60 publications

Genome and time-of-day transcriptome ofWolffia australianalink morphological extreme minimization with un-gated plant growth

Genome and time-of-day transcriptome ofWolffia australianalink morphological extreme minimization with un-gated plant growth

A highly efficient protocol for transformingCuscuta reflexabased on artificially induced infection sites

Subtilase activity in the intrusive cells mediates haustorium maturation in parasitic plants

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