Fungal phytopathogen modulates plant and insect responses to promote its dissemination

Author(s)

Franco, Flavia P. ^[1] ; Tuler, Amanda C. ^[2] ; Gallan, Diego Z. ^[1] ; Goncalves, Felipe G. ^[2] ; Favaris, Arodi P. ^[2] ; Penaflor, V, Maria Fernanda G. ; Leal, Walter S. ^[3] ; Moura, Daniel S. ^[4] ; Bento, Jose Mauricio S. ^[2] ; Silva-Filho, Marcio C. ^[1]

Affiliation

^[1] Univ Sao Paulo, Dept Genet, Escola Super Agr Luiz de Queiroz, Piracicaba, SP - Brazil

^[2] Univ Sao Paulo, Dept Entomol & Acarol, Escola Super Agr Luiz de Queiroz, Piracicaba, SP - Brazil

^[3] Univ Calif Davis, Dept Mol & Cellular Biol, Davis, CA 95616 - USA

^[4] Univ Sao Paulo, Dept Ciencias Biol, Escola Super Agr Luiz de Queiroz, Piracicaba, SP - Brazil

• Document type: Journal article
• Source: ISME Journal; v. 15, n. 12, p. 3522-3533, DEC 2021.
• Web of Science Citations: 2

Abstract

Vector-borne plant pathogens often change host traits to manipulate vector behavior in a way that favors their spread. By contrast, infection by opportunistic fungi does not depend on vectors, although damage caused by an herbivore may facilitate infection. Manipulation of hosts and vectors, such as insect herbivores, has not been demonstrated in interactions with fungal pathogens. Herein, we establish a new paradigm for the plant-insect-fungus association in sugarcane. It has long been assumed that Fusarium verticillioides is an opportunistic fungus, where it takes advantage of the openings left by Diatraea saccharalis caterpillar attack to infect the plant. In this work, we show that volatile emissions from F. verticillioides attract D. saccharalis caterpillars. Once they become adults, the fungus is transmitted vertically to their offspring, which continues the cycle by inoculating the fungus into healthy plants. Females not carrying the fungus prefer to lay their eggs on fungus-infected plants than mock plants, while females carrying the fungus prefer to lay their eggs on mock plants than fungus-infected plants. Even though the fungus impacts D. saccharalis sex behavior, larval weight and reproduction rate, most individuals complete their development. Our data demonstrate that the fungus manipulates both the host plant and insect herbivore across life cycle to promote its infection and dissemination. (AU)

• FAPESP's process: 17/08026-0 - Study of the interaction between sugar cane, D. saccharalis, C. falcatum and F. verticillioides
• Grantee: Diego Zanardo Gallan
• Support Opportunities: Scholarships in Brazil - Master
• FAPESP's process: 14/50871-0 - INCT 2014: National Institute of Science and Technology of Semiochemicals in Agriculture
• Grantee: José Roberto Postali Parra
• Support Opportunities: Research Projects - Thematic Grants
• FAPESP's process: 14/50275-9 - Deciphering the molecular mechanisms involved in the localization of organelar proteins as well as the complex plant-insect-pathogen interactions
• Grantee: Márcio de Castro Silva Filho
• Support Opportunities: Program for Research on Bioenergy (BIOEN) - Thematic Grants
• FAPESP's process: 13/12577-0 - Study of the molecular basis of SUGARWIN action in phytopathogenic fungi
• Grantee: Flávia Pereira Franco
• Support Opportunities: Scholarships in Brazil - Doctorate