Secreted Effector Proteins of Poplar Leaf Spot and Stem Canker Pathogen Sphaerulina musiva Manipulate Plant Immunity and Contribute to Virulence in Diverse Ways

Yao Zhao; Xinyue Zheng; Javier F. Tabima; Sheng Zhu; Kelsey L. Søndreli; Hope Hundley; Diane Bauer; Kerrie Barry; Yaxin Zhang; Jeremy Schmutz; Yuanchao Wang; Jared M. LeBoldus; Qin Xiong

doi:10.1094/MPMI-07-23-0091-R

Molecular Plant-Microbe Interactions (Dec 2023)

Secreted Effector Proteins of Poplar Leaf Spot and Stem Canker Pathogen Sphaerulina musiva Manipulate Plant Immunity and Contribute to Virulence in Diverse Ways

Yao Zhao,
Xinyue Zheng,
Javier F. Tabima,
Sheng Zhu,
Kelsey L. Søndreli,
Hope Hundley,
Diane Bauer,
Kerrie Barry,
Yaxin Zhang,
Jeremy Schmutz,
Yuanchao Wang,
Jared M. LeBoldus,
Qin Xiong

Affiliations

Yao Zhao: Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China
Xinyue Zheng: Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210095, China
Javier F. Tabima: Department of Botany and Plant Pathology, College of Agricultural Sciences, Oregon State University, Corvallis, OR 97331, U.S.A.
Sheng Zhu: Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210095, China
Kelsey L. Søndreli: Department of Botany and Plant Pathology, College of Agricultural Sciences, Oregon State University, Corvallis, OR 97331, U.S.A.
Hope Hundley: U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, U.S.A.
Diane Bauer: U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, U.S.A.
Kerrie Barry: U.S. Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, U.S.A.
Yaxin Zhang: Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210095, China
Jeremy Schmutz: HudsonAlpha Institute for Biotechnology, Huntsville, AL 35806, U.S.A.
Yuanchao Wang: Department of Plant Pathology, Nanjing Agricultural University, Nanjing 210095, China
Jared M. LeBoldus: Department of Botany and Plant Pathology, College of Agricultural Sciences, Oregon State University, Corvallis, OR 97331, U.S.A.
Qin Xiong: Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210095, China

DOI: https://doi.org/10.1094/MPMI-07-23-0091-R
Journal volume & issue: Vol. 36, no. 12
pp. 779 – 795

Abstract

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Fungal effectors play critical roles in manipulating plant immune responses and promoting colonization. Sphaerulina musiva is a heterothallic ascomycete fungus that causes Septoria leaf spot and stem canker disease in poplar (Populus spp.) plantations. This disease can result in premature defoliation, branch and stem breakage, increased mortality, and plantation failure. However, little is known about the interaction between S. musiva and poplar. Previous work predicted 142 candidate secreted effector proteins in S. musiva (SmCSEPs), 19 of which were selected for further functional characterization in this study. SmCSEP3 induced plant cell death in Nicotiana benthamiana, while 8 out of 19 tested SmCSEPs suppressed cell death. The signal peptides of these eight SmCSEPs exhibited secretory activity in a yeast signal sequence trap assay. Confocal microscopy revealed that four of these eight SmCSEPs target both the cytoplasm and the nucleus, whereas four predominantly localize to discrete punctate structures. Pathogen challenge assays in N. benthamiana demonstrated that the transient expression of six SmCSEPs promoted Fusarium proliferatum infection. The expression of these six SmCSEP genes were induced during infection. SmCSEP2, SmCSEP13, and SmCSEP25 suppressed chitin-triggered reactive oxygen species burst and callose deposition in N. benthamiana. The candidate secreted effector proteins of S. musiva target multiple compartments in the plant cell and modulate different pattern-triggered immunity pathways. [Graphic: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 “No Rights Reserved” license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2023.

Published in Molecular Plant-Microbe Interactions

ISSN: 0894-0282 (Print); 1943-7706 (Online)
Publisher: The American Phytopathological Society
Country of publisher: United States
LCC subjects: Science: Microbiology; Science: Botany
Website: https://apsjournals.apsnet.org/journal/mpmi

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