Interspecies hormonal control of host root morphology by parasitic plants

Abstract

Parasitic plants share a common anatomical feature, the haustorium. Haustoria enable both infection and nutrient transfer, which often leads to growth penalties for host plants and yield reduction in crop species. Haustoria also reciprocally transfer substances, such as RNA and proteins, from parasite to host, but the biological relevance for such movement remains unknown. Here, we studied such interspecies transport by using the hemiparasitic plant Phtheirospermum japonicum during infection of Arabidopsis thaliana. Tracer experiments revealed a rapid and efficient transfer of carboxyfluorescein diacetate (CFDA) from host to parasite upon formation of vascular connections. In addition, Phtheirospermum induced hypertrophy in host roots at the site of infection, a form of enhanced secondary growth that is commonly observed during various parasitic plant-host interactions. The plant hormone cytokinin is important for secondary growth, and we observed increases in cytokinin and its response during infection in both host and parasite. Phtheirospermum-induced host hypertrophy required cytokinin signaling genes (AHK3,4) but not cytokinin biosynthesis genes (IPT1,3,5,7) in the host. Furthermore, expression of a cytokinin-degrading enzyme in Phtheirospermum prevented host hypertrophy. Wild-type hosts with hypertrophy were smaller than ahk3,4 mutant hosts resistant to hypertrophy, suggesting hypertrophy improves the efficiency of parasitism. Taken together, these results demonstrate that the interspecies movement of a parasite-derived hormone modified both host root morphology and fitness. Several microbial and animal plant pathogens use cytokinins during infections, highlighting the central role of this growth hormone during the establishment of plant diseases and revealing a common strategy for parasite infections of plants.cytokinin | transport | hypertrophy | parasitism | Arabidopsis P arasitic plants are widespread agricultural pests and account for ∼1% of known flowering plants species (1). Parasitism ranges from holoparasites, which depend entirely on nutrient supply from host plants, to hemiparasites, which obtain nutrients via their own photosynthesis and from their hosts (1). Many hemiparasites do not depend on parasitism but often parasitize when conditions are suitable. These hemiparasitic plants include parasitic plants such as the commonly studied Orobanchaceae species Rhinanthus minor, Triphysaria versicolor, and Phtheirospermum japonicum. Both hemiparasites and holoparasites form specialized organs called haustoria that undergo a developmental transition from proto-haustoria to mature haustoria during the penetration and infection of host tissues to acquire nutrients and water (2). Some parasitic plants such as Striga or Rhinanthus form vascular connections exclusively to host xylem via xylem bridges (xylem-feeding), whereas haustoria of other plants such as Cuscuta or Orobanche also form symplastic phloem-to-phloem connections to host plants (phloem-feeding) (1). In addition to water and nutrients, other ...

Host lignin composition affects haustorium induction in the parasitic plants Phtheirospermum japonicum and Striga hermonthica

“…In addition, we tested the Arabidopsis F5H-knockout mutant (f5hKO), in which concentrations of S-type lignins were depleted to almost zero and concentrations of G-type lignins were substantially increased to c. 99% (Chapple et al, 1992;Meyer et al, 1998;Anderson et al, 2015). Arabidopsis is a host for P. japonicum but not for S. hermonthica, although S. hermonthica is able to form a haustorium and penetrate into Arabidopsis roots (Yoshida & Shirasu, 2009;Spallek et al, 2017). The shoot or root extracts of the Arabidopsis f5hKO plants exhibited significantly less haustorium induction in P. japonicum compared with that from WT plants (Fig.…”

“…Orobanchaceae parasitic plants form a multicellular organ, called a haustorium, which is essential in allowing parasites to invade host tissues and establish vascular connections Yoshida et al, 2016;Spallek et al, 2017). Facultative parasites including Phtheirospermum, Triphysaria and Agalinis spp.…”

The bacterial microbiota of a parasitic plant and its host

“…The haustorium attaches to the root or stem vasculature of host plants and acts as a 41 conduit through which material is exchanged primarily from host to parasite 42 (Sareendenchai and Zidorn 2008;LeBlanc et al, 2012;Spallek et al, 2017). 43…”

“…Plant immunological responses can re-structure 67 associated microbiota due to variation in the susceptibility of microbial taxa to plant 68 immune outputs (Lebeis et al, 2015;Stringlis et al, 2018;Voges et al, 2019). Finally, 69 parasitic plant-derived molecules can alter host root growth (Spallek et al, 2017), which 70 could alter the composition of associated microbiota. Thus, by altering the quality and 71 quantity of plant-derived resources available for microbes, activating innate plant 72 immunity, and altering host plant morphology, parasitic plant infection could perturb the 73 resident microbiota of their hosts.…”

“…Holoparasitic plants obtain their requisite energy, nutrients, and water from their hosts 391 by way of haustoria, which also allow symplastic and apoplastic transfer of nucleic acids, 392 proteins, and microorganisms (LeBlanc et al, 2012;Spallek et al, 2017). Consequently, 393 the assembly of parasitic plant microbiota is likely shaped by factors associated with 394 host plants (Sheng-Liang et al, 2014;Kruh et al, 2017;Cui et al, 2018).…”