Host-parasite tissue adhesion by a secreted type of β-1,4-glucanase in the parasitic plantPhtheirospermum japonicum

Abstract

Tissue adhesion between plant species occurs both naturally and artificially. Parasitic plants establish symbiotic relationship with host plants by adhering tissues at roots or stems. Plant grafting, on the other hand, is a widely used technique in agriculture to adhere tissues of two stems. While compatibility of tissue adhesion in plant grafting is often limited within close relatives, parasitic plants exhibit much wider compatibilities. For example, the Orobanchaceae parasitic plant Striga hermonthica is able to infect Poaceae crop plants, causing a serious agricultural loss. Here we found that the model Orobanchaceae parasite plant Phtheirospermum japonicum can be grafted on to interfamily species, such as Arabidopsis, a Brassicaceae plant. To understand molecular basis of tissue adhesion between distant plant species, we conducted comparative transcriptome analyses on both infection and grafting by P. japonicum on Arabidopsis. Through gene clustering, we identified genes upregulated during these tissue adhesion processes, which include cell proliferation- and cell wall modification-related genes. By comparing with a transcriptome dataset of interfamily grafting between Nicotiana and Arabidopsis, we identified 9 genes commonly induced in tissue adhesion between distant species. Among them, we showed a gene encoding secreted type of β-1,4-glucanase plays an important role for plant parasitism. Our data provide insights into the molecular commonality between parasitism and grafting in plants.Significance StatementComprehensive sequential RNA-Seq datasets for parasitic infection of the root and grafting of the stem between P. japonicum and Arabidopsis revealed that molecular events of parasitism and grafting are substantially different and only share a part of events such as cell proliferation and cell wall modification. This study demonstrated that a secreted type of β-1,4-glucanase gene expressed in cells located at the parasite–host interface as an important factor for parasitism in the Orobanchaceae.

Orobanchaceae parasite–host interactions

“…These data suggest that the tissue adhesion process in parasitism is similar to that in artificial grafting, an agricultural technique used to adhere the tissues of two different stems enzymatically (Notaguchi et al ., 2020). Indeed, comparative transcriptome analysis of parasitism and grafting using P. japonicum and Arabidopsis identified GH9B3 gene homologs, encoding β‐1,4‐glucanases, as commonly upregulated during the tissue adhesion process (Kurotani et al ., 2020). Furthermore, knockdown of GH93B results in both an increased number of impaired haustoria and an increased number of grafting failures, suggesting that GH9B is an important component for both parasitism and grafting (Kurotani et al ., 2020; Notaguchi et al ., 2020).…”

Anin vitrografting method to quantify mechanical forces of adhering tissues

“…We recently uncovered a key role of the GH9B3 clade of β-1,4-glucanases in cell-cell adhesion at the graft junction (Notaguchi et al 2020;Kurotani et al 2020). β-1,4-glucanases probably target cellulose in cell walls, and the overexpression of the β-1,4-glucanase gene promotes graft efficiency in Arabidopsis (Notaguchi et al 2020).…”

“…Using this system, we first showed that exogenous treatment with cellulases promotes graft adhesion. Given that numerous candidate genes related to grafting have been identified through recent transcriptome analyses (Cookson et al 2014;Liu et al 2015;Melnyk et al 2015;Li et al 2016;Chen et al 2017;Wang et al 2019;Xie et al 2019;Kurotani et al 2020;Notaguchi et al 2020 Figure 3C). In both cases, no correlation was observed between adhesive force and graft area.…”

“…In regard to molecular mechanisms, studies have revealed the activity of enzymes, such as peroxidase and catalase, during grafting (Fernández-garcía et al 2004;Pina and Errea 2008;Irisarri et al 2015). Molecular genetic studies of grafting have been conducted in fruit trees, vegetables, and model plants (Cookson et al 2014;Wang et al 2014;Liu et al 2015;Melnyk et al 2015;Irisarri et al 2015;Li et al 2016;Matsuoka et al 2016;Chen et al 2017;Melnyk et al 2016;Matsuoka et al 2018;Wang et al 2019;Xie et al 2019;Kurotani et al 2020;Notaguchi et al 2020). Among the various findings, these studies have clearly shown that grafting is promoted by auxin action through the expression of genes related to auxin signaling.…”

“…Among the various findings, these studies have clearly shown that grafting is promoted by auxin action through the expression of genes related to auxin signaling. The phytohormone auxin is transported basipetally from synthetic tissues, such as leaves and buds, by polar transport and accumulates at the damaged site (Yin et al 2012;Wang et al 2014;Liu et al 2015;Melnyk et al 2015;Matsuoka et al 2016;Chen et al 2017;Melnyk et al 2016;Kurotani et al 2020;Notaguchi et al 2020). Auxin promotes the formation of vascular strands when applied exogenously to undifferentiated tissue (Parkinson and Yeoman 1982;Wang et al 2014).…”