G protein α subunit suppresses sporangium formation through a serine/threonine protein kinase in Phytophthora sojae

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Abstract
Eukaryotic heterotrimeric guanine nucleotide-binding proteins consist of α, β, and γ subunits, which act as molecular switches to regulate a number of fundamental cellular processes. In the oomycete pathogen Phytophthora sojae, the sole G protein α subunit (Gα; encoded by PsGPA1) has been found to be involved in zoospore mobility and virulence, but how it functions remains unclear. In this study, we show that the Gα subunit PsGPA1 directly interacts with PsYPK1, a serine/threonine protein kinase that consists of an N-terminal region with unknown function and a C-terminal region with a conserved catalytic kinase domain. We generated knockout and knockout-complemented strains of PsYPK1 and found that deletion of PsYPK1 resulted in a pronounced reduction in the production of sporangia and oospores, in mycelial growth on nutrient poor medium, and in virulence. PsYPK1 exhibits a cytoplasmic-nuclear localization pattern that is essential for sporangium formation and virulence of P. sojae. Interestingly, PsGPA1 overexpression was found to prevent nuclear localization of PsYPK1 by exclusively binding to the N-terminal region of PsYPK1, therefore accounting for its negative role in sporangium formation. Our data demonstrate that PsGPA1 negatively regulates sporangium formation by repressing the nuclear localization of its downstream kinase PsYPK1. Eukaryotic heterotrimeric guanine nucleotide-binding proteins consist of α, β, and γ subunits, which act as molecular switches to regulate a number of fundamental cellular processes. In oomycete plant pathogen Phytophthora sojae, previous research showed that G protein α subunit is involved in zoospore motility and pathogenicity. However, the elaborate functions of the G protein α subunit remain largely unknown. Here, we identified a serine/threonine protein kinase, PsYPK1, which directly interacts with the G protein α subunit (PsGPA1) in P. sojae. We found that PsYPK1 regulates the production of sporangia and oospores, mycelial growth in nutrient poor medium, and pathogenicity in P. sojae. We further revealed that PsYPK1 exhibits a cytoplasmic-nuclear localization pattern that is essential for sporangium formation and pathogenicity of P. sojae. Interestingly, PsGPA1 overexpression was found to prevent nuclear localization of PsYPK1 by exclusively binding to the N-terminal region of PsYPK1, accounting for the negative role of PsGPA1 in sporangium formation. Our study is the first to show that G protein signaling is transmitted to a downstream effector to regulate the development and pathogenicity of an oomycete pathogen, which opens new avenues for researches on animal and plant pathogens and host-microbe interactions.
Funding Information
  • National Natural Science Foundation of China (31721004)
  • International Science and Technology Cooperation Programme (2013DFG32030)
  • Key Technologies Research and Development Program (2018YFD0201000)
  • National Natural Science Foundation of China (31772140)

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