Autophagy-Related Gene PlATG6a Is Involved in Mycelial Growth, Asexual Reproduction and Tolerance to Salt and Oxidative Stresses in Peronophythora litchii

Abstract

Autophagy is ubiquitously present in eukaryotes. During this process, intracellular proteins and some waste organelles are transported into lysosomes or vacuoles for degradation, which can be reused by the cell to guarantee normal cellular metabolism. However, the function of autophagy-related (ATG) proteins in oomycetes is rarely known. In this study, we identified an autophagy-related gene, PlATG6a, encoding a 514-amino-acid protein in Peronophythora litchii, which is the most destructive pathogen of litchi. The transcriptional level of PlATG6a was relatively higher in mycelium, sporangia, zoospores and cysts. We generated PlATG6a knockout mutants using CRISPR/Cas9 technology. The P. litchii Δplatg6a mutants were significantly impaired in autophagy and vegetative growth. We further found that the Δplatg6a mutants displayed decreased branches of sporangiophore, leading to impaired sporangium production. PlATG6a is also involved in resistance to oxidative and salt stresses, but not in sexual reproduction. The transcription of peroxidase-encoding genes was down-regulated in Δplatg6a mutants, which is likely responsible for hypersensitivity to oxidative stress. Compared with the wild-type strain, the Δplatg6a mutants showed reduced virulence when inoculated on the litchi leaves using mycelia plugs. Overall, these results suggest a critical role for PlATG6a in autophagy, vegetative growth, sporangium production, sporangiophore development, zoospore release, pathogenesis and tolerance to salt and oxidative stresses in P. litchii.

MdHB7‐like positively modulates apple salt tolerance by promoting autophagic activity and Na+ efflux

“…Autophagy is a protein degradation process in which cells recycle cytoplasmic contents under environmental stress or during particular developmental stages (Zhou, Wang, et al., 2014). Environmental stressors, such as drought, salt, and high temperature, lead to the production of harmful proteins and damaged organelles, and autophagy degrades these damaged intracellular components to maintain homeostasis in the cell microenvironment and promote the reuse of some substances, thus enhancing stress tolerance (Bao et al., 2020; Chen et al., 2015; Wang et al., 2022; Yang et al., 2020; Yue et al., 2022; Zhang, Zhou, et al., 2022; Zhou, Zhang, et al., 2014). Studies in several plant species have shown that overexpressing various ATG genes increases autophagic activity in transgenic plants, thereby enhancing stress tolerance (Wang et al., 2015, 2022; Zhang, Zhou, et al., 2022; Zhou, Wang, et al., 2014).…”

“…Environmental stressors, such as drought, salt, and high temperature, lead to the production of harmful proteins and damaged organelles, and autophagy degrades these damaged intracellular components to maintain homeostasis in the cell microenvironment and promote the reuse of some substances, thus enhancing stress tolerance (Bao et al., 2020; Chen et al., 2015; Wang et al., 2022; Yang et al., 2020; Yue et al., 2022; Zhang, Zhou, et al., 2022; Zhou, Zhang, et al., 2014). Studies in several plant species have shown that overexpressing various ATG genes increases autophagic activity in transgenic plants, thereby enhancing stress tolerance (Wang et al., 2015, 2022; Zhang, Zhou, et al., 2022; Zhou, Wang, et al., 2014). In apples, several MdATG genes that respond to abiotic stress and are involved in regulating autophagic activity and stress tolerance have been identified, such as MdATG5a (Jia, Jia, et al., 2021), MdATG8i (Huo, Guo, Wang, et al., 2020; Jia, Gong, et al., 2021; Jia, Mao, et al., 2021), MdATG10 (Huo, Guo, Jia, et al., 2020), MdATG9 (Huo, Guo, Zhang, et al., 2020), and MdATG18a (Huo et al., 2020; Li et al., 2020; Sun, Jia, et al., 2018; Sun, Wang, et al., 2018).…”

“…Autophagy is a housekeeping pathway and is quickly induced by a variety of stressors, such as drought (Bao et al., 2020; Jia, Jia, et al., 2021; Sun, Wang, et al., 2018; Wang et al., 2015), salt stress (Huo, Guo, Jia, et al., 2020; Luo et al., 2017), heat (Thirumalaikumar et al., 2021), nutrient starvation (Huang et al., 2019; Huo, Guo, Zhang, et al., 2020; Zhang, Zhou, et al., 2022), oxidative stress (Wang et al., 2022; Zhang, Wang, et al., 2021), ion imbalances (Shinozaki & Yoshimoto, 2021), and pathogen attack (Hafren & Hofius, 2017; Signorelli et al., 2019; Zhang, Shao, et al., 2021). Several lines of evidence suggest that upregulating the expression of ATG genes improves autophagic activity, thereby enhancing stress tolerance by promoting the degradation of damaged macromolecules or organelles, increasing antioxidant enzyme activities, and promoting the accumulation of osmoregulatory substances (Tang & Bassham, 2022; Thanthrige et al., 2021; Wang, Cao, et al., 2019).…”

UvATG6 Interacts with BAX Inhibitor 1 Proteins and Plays Critical Roles in Growth, Conidiation, and Virulence in Ustilaginoidea virens

“…FgATG6 is required for growth and virulence in Fusarium graminearum ( 33 ). In Peronophythora litchii , PlATG6a is involved in growth, asexual reproduction, and stress tolerance ( 34 ). In addition, several ATGs in U. virens , including UvATG8 , UvATG7 , and UvATG14 , have been characterized as being involved in growth, conidiation, and virulence ( 24 – 26 ).…”

Autophagy-related protein PlATG2 regulates the vegetative growth, sporangial cleavage, autophagosome formation, and pathogenicity of peronophythora litchii

“…Studies have shown that autophagy is essential for the development of P. infestans and P. sojae [ 34 , 35 ]. Deletion of ATG6a homologs PsATG6a and PlATG6a attenuated autophagosome formation and decreased the pathogenicity of P. sojae and P. litchii on soybean and litchi, respectively [ 34 , 36 ]. In addition, PsATG2 displayed a higher transcription level during the infection stage in P. sojae [ 34 ], indicating that PsATG2 probably participates in the virulence of P. sojae .…”