Interspecies hormonal control of host root morphology by parasitic plants

Proc Natl Acad Sci U S A. 2017 May 16;114(20):5283-5288. doi: 10.1073/pnas.1619078114. Epub 2017 May 1.

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.

Keywords: Arabidopsis; cytokinin; hypertrophy; parasitism; transport.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis / parasitology*
  • Arabidopsis Proteins / metabolism
  • Cytokinins / metabolism
  • Cytokinins / physiology*
  • Host-Parasite Interactions
  • Orobanchaceae / metabolism
  • Orobanchaceae / physiology*
  • Parasites
  • Plant Diseases / parasitology
  • Plant Growth Regulators / metabolism
  • Plant Growth Regulators / physiology*
  • Plant Roots / cytology
  • Plant Roots / metabolism
  • Plants
  • Signal Transduction
  • Symbiosis / physiology

Substances

  • Arabidopsis Proteins
  • Cytokinins
  • Plant Growth Regulators