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Sts2, a transcriptional activator effector of Ustilago maydis, regulates hyperplasia in maize during pathogen-induced tumor formation

ABSTRACT: Ustilago maydis causes common smut in maize, which is characterized by tumor formation in aerial parts of maize. Tumor comes from the de novo cell division of highly developed bundle sheath and subsequent cell enlargement. However, its mechanism is still unknown. Here, we characterize the U. maydis effector Sts2 (Small tumor on seedlings 2), which promotes the division of hyperplasia tumor cells. Upon infection, Sts2 is translocated into maize cell nucleus, where it acts as a transcriptional activator, and the transactivation activity is crucial for its virulence function. Sts2 interacts with ZmNECAP1, a yet undescribed plant transcriptional activator, and it activates the expression of several leaf developmental regulators to potentiate tumor formation. Contrary, a suppressive Sts2-SRDX inhibits the tumor formation by SG200 in a dominant negative way, underpinning the central role of Sts2 for tumorigenesis. Our results not only disclosed the virulence mechanism of a tumorigenic effector, but also revealed the essential role of leaf developmental regulators in pathogen-induced tumor formation.

INSTRUMENT(S): Q Exactive

ORGANISM(S): Zea Mays (maize)

TISSUE(S): Plant Cell

SUBMITTER: Sara Christina Stolze

LAB HEAD: Hirofumi Nakagami

PROVIDER: PXD040350 | Pride | 2023-10-12

REPOSITORIES: Pride

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Project description:Many of the genes coding for secreted protein effectors are arranged in gene clusters in the genome of the biotrophic plant pathogen Ustilago maydis. The largest of these gene clusters, cluster 19A, encodes 24 secreted effectors. Deletion of the entire cluster results in severe attenuation of virulence. The generation and analysis strains carrying sub-deletions identified 9 genes significantly contributing to tumor formation after seedling infection. As the individual contributions of these genes to tumor formation were small, we studied the response of maize plants to the whole cluster mutant as well as to several individual mutants by array analysis. This revealed distinct plant responses, demonstrating that the respective effectors have discrete plant targets. Many of the genes coding for secreted protein effectors are arranged in gene clusters in the genome of the biotrophic plant pathogen Ustilago maydis. The largest of these gene clusters, cluster 19A, encodes 24 secreted effectors. Deletion of the entire cluster results in severe attenuation of virulence. The generation and analysis strains carrying sub-deletions identified 9 genes significantly contributing to tumor formation after seedling infection. As the individual contributions of these genes to tumor formation were small, we studied the response of maize plants to the whole cluster mutant as well as to several individual mutants by array analysis. This revealed distinct plant responses, demonstrating that the respective effectors have discrete plant targets. We used the Affymetrix maize genome array to analyze the transcriptional responses of maize to cluster 19A mutants and individual sub-deletions for the cluster 19A genes tin1, tin3, tin4 and tin5. We found plant responses to the mutants were significantly different although the macroscopic phenotypes of the individual mutants were very similar. U. maydis infected parts of maize seedling leaves were dissected 4 days after inoculation with strain SG200∆19A, SG200∆tin1, SG200∆tin3, SG200∆tin4 and SG200∆tin5, respectively. We previously submitted data of maize leaves that were treated with the progenitor wild type strain SG200 as well as mock-infections under identical experimetal conditions (GEO: GSE10023). These data served as controls for this experiment.

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	190605_GD_WeZu_B_01.raw	Raw
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	190605_GD_WeZu_B_03.raw	Raw
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	190605_GD_WeZu_B_05.raw	Raw

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Sts2, a transcriptional activator effector of Ustilago maydis, regulates hyperplasia in maize during pathogen-induced tumor formation

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