Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens
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Evaluation Summary:
The study provides evidence that PEN1 and SYP122 regulate defense structures against filamentous pathogen infection including papillae formation and encasement of haustoria; this appears to be an ancient defense mechanism in land plants. If the findings that PEN1 and its close homolog SYP122 play an overlapping role in pre- and post-invasive immunity against cell-wall penetrating filamentous pathogens could be further validated, this would advance our understanding of callosic papilla/encasement-based nonhost defense mechanisms.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Abstract
Filamentous fungal and oomycete plant pathogens that invade by direct penetration through the leaf epidermal cell wall cause devastating plant diseases. Plant preinvasive immunity toward nonadapted filamentous pathogens is highly effective and durable. Pre- and postinvasive immunity correlates with the formation of evolutionarily conserved and cell-autonomous cell wall structures, named papillae and encasements, respectively. Yet, it is still unresolved how papillae/encasements are formed and whether these defense structures prevent pathogen ingress. Here, we show that in Arabidopsis the two closely related members of the SYP12 clade of syntaxins (PEN1 and SYP122) are indispensable for the formation of papillae and encasements. Moreover, loss-of-function mutants were hampered in preinvasive immunity toward a range of phylogenetically distant nonadapted filamentous pathogens, underlining the versatility and efficacy of this defense. Complementation studies using SYP12s from the early diverging land plant, Marchantia polymorpha , showed that the SYP12 clade immunity function has survived 470 million years of independent evolution. These results suggest that ancestral land plants evolved the SYP12 clade to provide a broad and durable preinvasive immunity to facilitate their life on land and pave the way to a better understanding of how adapted pathogens overcome this ubiquitous plant defense strategy.
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Evaluation Summary:
The study provides evidence that PEN1 and SYP122 regulate defense structures against filamentous pathogen infection including papillae formation and encasement of haustoria; this appears to be an ancient defense mechanism in land plants. If the findings that PEN1 and its close homolog SYP122 play an overlapping role in pre- and post-invasive immunity against cell-wall penetrating filamentous pathogens could be further validated, this would advance our understanding of callosic papilla/encasement-based nonhost defense mechanisms.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 agreed to share their name with the authors.)
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Reviewer #2 (Public Review):
In this manuscript, the authors investigated the role of PEN1 and its close homolog SYP122 in pre- and post-invasive immunity reflected by the formation of papilla and haustorial encasement at the point of the attempted/sucessful penetration from non-adapted powdery and other filamentous pathogens. The authors collected genetic, cytological and cell biological data to show that these two syntaxins are required for the formation of the induced callosic defense structures. They further suggested that the two syntaxins function redundantly and differently. PEN1 may possess two different functions: the first is to mediate rapid delivery of papilla materials to powdery mildew penetration site, which is unique and not shared by SYP122, and the second is to work along with SYP122 to enable formation of a more …
Reviewer #2 (Public Review):
In this manuscript, the authors investigated the role of PEN1 and its close homolog SYP122 in pre- and post-invasive immunity reflected by the formation of papilla and haustorial encasement at the point of the attempted/sucessful penetration from non-adapted powdery and other filamentous pathogens. The authors collected genetic, cytological and cell biological data to show that these two syntaxins are required for the formation of the induced callosic defense structures. They further suggested that the two syntaxins function redundantly and differently. PEN1 may possess two different functions: the first is to mediate rapid delivery of papilla materials to powdery mildew penetration site, which is unique and not shared by SYP122, and the second is to work along with SYP122 to enable formation of a more general papilla/encasement in response to filamentous pathogens, and the latter is evolutionarily conserved as SYP12a from Marchantia can compensate the loss of SYP122.
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Reviewer #1 (Public Review):
In this study the authors show that PEN1 and its close paralog SYP122 are required for pre-invasive (papillae formation) and invasive immunity (encasement of haustoria) against non-adapted powdery mildew fungal infection. Importantly, papillae formation on plants challenged with C. destructivum and P. infestans also required PEN1 and SYP122, suggesting that defense structures determined by the PEN1 and SYP122 operate against diverse filamentous pathogens. In addition, the authors provide strong evidence that the function specified by PEN1/SYP122 also exist in M. polymorpha, indicating an ancient evolution of the pre-invasive/invasive structures. Overall, the study makes a strong case that PEN1 and SYP122 play a crucial role in the biogenesis of ancient defense structures.
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