Homeostasis of cell wall integrity pathway phosphorylation is required for the growth and pathogenicity of <i>Magnaporthe oryzae</i>

Cai, Yongchao; Liu, Xinyu; Shen, Lingbo; Wang, Nian; He, Yangjie; Zhang, Haifeng; Wang, Ping

doi:10.1111/mpp.13225

Cited by 5 publications

(2 citation statements)

References 55 publications

(84 reference statements)

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“…However, constitutively activated CWI signaling disrupts the balance between growth and stress response. Previous studies also showed that phosphatases MoPtc1 and MoPtc2 dephosphorylate MoMkk1 to switch off CWI signaling ( 13 ). Moreover, studies indicated that the MAPK cascade plays a role in CWI signaling and autophagy, which is regulated by MAPK pathways in response to external stimuli or environmental conditions ( 14 ).…”

Section: Introductionmentioning

confidence: 89%

MoMkk1 and MoAtg1 dichotomously regulating autophagy and pathogenicity through MoAtg9 phosphorylation in Magnaporthe oryzae

Kong,

Guo,

et al. 2024

mBio

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Autophagy is a central biodegradation pathway critical in eliminating intracellular cargo to maintain cellular homeostasis and improve stress resistance. At the same time, the key component of the mitogen-activated protein kinase cascade regulating cell wall integrity signaling MoMkk1 has an essential role in the autophagy of the rice blast fungus Magnaporthe oryzae . Still, the mechanism of how MoMkk1 regulates autophagy is unclear. Interestingly, we found that MoMkk1 regulates the autophagy protein MoAtg9 through phosphorylation. MoAtg9 is a transmembrane protein subjected to phosphorylation by autophagy-related protein kinase MoAtg1. Here, we provide evidence demonstrating that MoMkk1-dependent MoAtg9 phosphorylation is required for phospholipid translocation during isolation membrane stages of autophagosome formation, an autophagic process essential for the development and pathogenicity of the fungus. In contrast, MoAtg1-dependent phosphorylation of MoAtg9 negatively regulates this process, also impacting growth and pathogenicity. Our studies are the first to demonstrate that MoAtg9 is subject to MoMkk1 regulation through protein phosphorylation and that MoMkk1 and MoAtg1 dichotomously regulate autophagy to underlie the growth and pathogenicity of M. oryzae . IMPORTANCE Magnaporthe oryzae utilizes multiple signaling pathways to promote colonization of host plants. MoMkk1, a cell wall integrity signaling kinase, plays an essential role in autophagy governed by a highly conserved autophagy kinase MoAtg1-mediated pathway. How MoMkk1 regulates autophagy in coordination with MoAtg1 remains elusive. Here, we provide evidence that MoMkk1 phosphorylates MoAtg9 to positively regulate phospholipid translocation during the isolation membrane or smaller membrane structures stage of autophagosome formation. This is in contrast to the negative regulation of MoAtg9 by MoAtg1 for the same process. Intriguingly, MoMkk1-mediated MoAtg9 phosphorylation enhances the fungal infection of rice, whereas MoAtg1-dependant MoAtg9 phosphorylation significantly attenuates it. Taken together, we revealed a novel mechanism of autophagy and virulence regulation by demonstrating the dichotomous functions of MoMkk1 and MoAtg1 in the regulation of fungal autophagy and pathogenicity.

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Section: Introductionmentioning

confidence: 89%

MoMkk1 and MoAtg1 dichotomously regulating autophagy and pathogenicity through MoAtg9 phosphorylation in Magnaporthe oryzae

Kong,

Guo,

et al. 2024

mBio

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“…The plant cell wall, a complex network of polysaccharides, including cellulose, hemicellulose, and pectin ( 3 – 5 ), is the initial physical and defensive barrier against a variety of biological stresses and is thus an important site of host-pathogen interaction ( 5 , 6 ). Plant cell walls usually participate in the immune response via dynamic remodeling to prevent pathogen infection ( 7 ); the plant cell wall also senses external stressors and transmits signals to stimulate defensive responses in the host ( 7 – 9 ).…”

Section: Introductionmentioning

confidence: 99%

Pectate Lyase from Fusarium sacchari Induces Plant Immune Responses and Contributes to Virulence

et al. 2023

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Involvement of the Cell Wall–Integrity Pathway in Signal Recognition, Cell-Wall Biosynthesis, and Virulence in Magnaporthe oryzae

Chen

Yang

et al. 2023

MPMI

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The fungal cell wall is the first layer exposed to the external environment. The cell wall has key roles in regulating cell functions, such as cellular stability, permeability, and protection against stress. Understanding the structure of the cell wall and the mechanism of its biogenesis is important for the study of fungi. Highly conserved in fungi including M. oryzae, the cell wall integrated (CWI) pathway is the primary signaling cascade regulating cell wall structure and function. The CWI pathway has been demonstrated to correlate with the pathogenicity in many phytopathogenic fungi. In the synthesis of cell wall, the CWI pathway cooperates with multiple signaling pathways to regulate cell morphogenesis and secondary metabolism. Many questions have arisen regarding the cooperation of different signaling pathways with the CWI pathway in regulating cell wall synthesis and pathogenicity. In this review, we summarized the latest advances in the M. oryzae CWI pathway and cell wall structure. We discussed the CWI pathway components and their involvement in different aspects, such as virulence factors, the possibility of the pathway as a target for antifungal therapies, and cross-talk with other signaling pathways. This information will aid in better understanding the universal functions of the CWI pathway in regulating cell wall synthesis and pathogenicity in M. oryzae.

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Homeostasis of cell wall integrity pathway phosphorylation is required for the growth and pathogenicity of Magnaporthe oryzae

Abstract: In M. oryzae, the cell wall integrity (CWI) pathway consists of the MAP kinase kinase kinase (MoMck1), the MAP kinase kinase (MoMkk1), and the MAP kinase (MoMps1).

Cited by 5 publications

References 55 publications

MoMkk1 and MoAtg1 dichotomously regulating autophagy and pathogenicity through MoAtg9 phosphorylation in Magnaporthe oryzae

MoMkk1 and MoAtg1 dichotomously regulating autophagy and pathogenicity through MoAtg9 phosphorylation in Magnaporthe oryzae

Pectate Lyase from Fusarium sacchari Induces Plant Immune Responses and Contributes to Virulence

Involvement of the Cell Wall–Integrity Pathway in Signal Recognition, Cell-Wall Biosynthesis, and Virulence in Magnaporthe oryzae

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