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

Author

Listed:
  • Weiliang Zuo

    (University of Cologne)

  • Jasper R. L. Depotter

    (University of Cologne
    The Francis Crick Institute)

  • Sara Christina Stolze

    (Max-Planck Institute for Plant Breeding Research)

  • Hirofumi Nakagami

    (Max-Planck Institute for Plant Breeding Research
    Max Planck Institute for Plant Breeding Research)

  • Gunther Doehlemann

    (University of Cologne)

Abstract

Ustilago maydis causes common smut in maize, which is characterized by tumor formation in aerial parts of maize. Tumors result from the de novo cell division of highly developed bundle sheath and subsequent cell enlargement. However, the molecular mechanisms underlying tumorigenesis are still largely 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 the 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. On the contrary, fusion of a suppressive SRDX-motif to Sts2 causes dominant negative inhibition of tumor formation, underpinning the central role of Sts2 for tumorigenesis. Our results not only disclose the virulence mechanism of a tumorigenic effector, but also reveal the essential role of leaf developmental regulators in pathogen-induced tumor formation.

Suggested Citation

  • Weiliang Zuo & Jasper R. L. Depotter & Sara Christina Stolze & Hirofumi Nakagami & Gunther Doehlemann, 2023. "A transcriptional activator effector of Ustilago maydis regulates hyperplasia in maize during pathogen-induced tumor formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42522-w
    DOI: 10.1038/s41467-023-42522-w
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    1. Johana C. Misas Villamil & André N. Mueller & Fatih Demir & Ute Meyer & Bilal Ökmen & Jan Schulze Hüynck & Marlen Breuer & Helen Dauben & Joe Win & Pitter F. Huesgen & Gunther Doehlemann, 2019. "A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    2. Seongbeom Kim & Chi-Yeol Kim & Sook-Young Park & Ki-Tae Kim & Jongbum Jeon & Hyunjung Chung & Gobong Choi & Seomun Kwon & Jaeyoung Choi & Junhyun Jeon & Jong-Seong Jeon & Chang Hyun Khang & Seogchan K, 2020. "Two nuclear effectors of the rice blast fungus modulate host immunity via transcriptional reprogramming," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    3. Armin Djamei & Kerstin Schipper & Franziska Rabe & Anupama Ghosh & Volker Vincon & Jörg Kahnt & Sonia Osorio & Takayuki Tohge & Alisdair R. Fernie & Ivo Feussner & Kirstin Feussner & Peter Meinicke & , 2011. "Metabolic priming by a secreted fungal effector," Nature, Nature, vol. 478(7369), pages 395-398, October.
    4. Lay-Sun Ma & Lei Wang & Christine Trippel & Artemio Mendoza-Mendoza & Steffen Ullmann & Marino Moretti & Alexander Carsten & Jörg Kahnt & Stefanie Reissmann & Bernd Zechmann & Gert Bange & Regine Kahm, 2018. "The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
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