SUPPRESSOR OF APICAL DOMINANCE1 of Sporisorium reilianum Modulates Inflorescence Branching Architecture in Maize and Arabidopsis.
The biotrophic fungus Sporisorium reilianum causes head smut of maize (Zea mays) after systemic plant colonization. Symptoms include the formation of multiple female inflorescences at subapical nodes of the stalk because of loss of apical dominance. By deletion analysis of cluster 19-1, the largest genomic divergence cluster in S. reilianum, we identified a secreted fungal effector responsible for S. reilianum-induced loss of apical dominance, which we named SUPPRESSOR OF APICAL DOMINANCE1 (SAD1). SAD1 transcript levels were highly up-regulated during biotrophic fungal growth in all infected plant tissues. SAD1-green fluorescent protein fusion proteins expressed by recombinant S. reilianum localized to the extracellular hyphal space. Transgenic Arabidopsis (Arabidopsis thaliana)-expressing green fluorescent protein-SAD1 displayed an increased number of secondary rosette-leaf branches. This suggests that SAD1 manipulates inflorescence branching architecture in maize and Arabidopsis through a conserved pathway. Using a yeast (Saccharomyces cerevisiae) two-hybrid library of S. reilianum-infected maize tissues, we identified potential plant interaction partners that had a predicted function in ubiquitination, signaling, and nuclear processes. Presence of SAD1 led to an increase of the transcript levels of the auxin transporter PIN-FORMED1 in the root and a reduction of the branching regulator TEOSINTE BRANCHED1 in the stalk. This indicates a role of SAD1 in regulation of apical dominance by modulation of branching through increasing transcript levels of the auxin transporter PIN1 and derepression of bud outgrowth.
Molecular Biology of Plant-Microbe Interactions (H.G., J.S.) andPlant Cell Biology (C.L., T.T.), Albrecht von Haller Institute of Plant Sciences, Georg August Universität Göttingen, 37077 Goettingen, Germany;Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany (H.G., J.S.);Department of Plant Biotechnology, National Research Centre, 12311 Cairo, Egypt (H.G.); andMicrobial Genetics, Institute of Applied Microbiology, Aachen Biology and Biotechnology, RWTH Aachen University, 52074 Aachen, Germany (F.D., J.S.).
Hassan
H
Ghareeb
Molecular Biology of Plant-Microbe Interactions (H.G., J.S.) andPlant Cell Biology (C.L., T.T.), Albrecht von Haller Institute of Plant Sciences, Georg August Universität Göttingen, 37077 Goettingen, Germany;Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany (H.G., J.S.);Department of Plant Biotechnology, National Research Centre, 12311 Cairo, Egypt (H.G.); andMicrobial Genetics, Institute of Applied Microbiology, Aachen Biology and Biotechnology, RWTH Aachen University, 52074 Aachen, Germany (F.D., J.S.).
Frank
http://orcid.org/0000-0003-2604-2148
F
Drechsler
Molecular Biology of Plant-Microbe Interactions (H.G., J.S.) andPlant Cell Biology (C.L., T.T.), Albrecht von Haller Institute of Plant Sciences, Georg August Universität Göttingen, 37077 Goettingen, Germany;Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany (H.G., J.S.);Department of Plant Biotechnology, National Research Centre, 12311 Cairo, Egypt (H.G.); andMicrobial Genetics, Institute of Applied Microbiology, Aachen Biology and Biotechnology, RWTH Aachen University, 52074 Aachen, Germany (F.D., J.S.).
Christian
C
Löfke
Molecular Biology of Plant-Microbe Interactions (H.G., J.S.) andPlant Cell Biology (C.L., T.T.), Albrecht von Haller Institute of Plant Sciences, Georg August Universität Göttingen, 37077 Goettingen, Germany;Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany (H.G., J.S.);Department of Plant Biotechnology, National Research Centre, 12311 Cairo, Egypt (H.G.); andMicrobial Genetics, Institute of Applied Microbiology, Aachen Biology and Biotechnology, RWTH Aachen University, 52074 Aachen, Germany (F.D., J.S.).
Thomas
T
Teichmann
Molecular Biology of Plant-Microbe Interactions (H.G., J.S.) andPlant Cell Biology (C.L., T.T.), Albrecht von Haller Institute of Plant Sciences, Georg August Universität Göttingen, 37077 Goettingen, Germany;Organismic Interactions, Max Planck Institute for Terrestrial Microbiology, 35043 Marburg, Germany (H.G., J.S.);Department of Plant Biotechnology, National Research Centre, 12311 Cairo, Egypt (H.G.); andMicrobial Genetics, Institute of Applied Microbiology, Aachen Biology and Biotechnology, RWTH Aachen University, 52074 Aachen, Germany (F.D., J.S.) jan.schirawski@rwth-aachen.de.
Jan
J
Schirawski
D000595:Amino Acid Sequence; D017360:Arabidopsis / Q000235:genetics* / Q000382:microbiology / Q000502:physiology; D001483:Base Sequence; D001692:Biological Transport / Q000235:genetics; D005656:Fungal Proteins / Q000235:genetics* / Q000378:metabolism; D005786:Gene Expression Regulation; D054884:Host-Pathogen Interactions / Q000235:genetics; D025301:Hyphae / Q000235:genetics / Q000378:metabolism; D007210:Indoleacetic Acids / Q000378:metabolism; D056626:Inflorescence / Q000235:genetics* / Q000378:metabolism / Q000502:physiology; D008164:Luminescent Proteins / Q000235:genetics / Q000378:metabolism; D018519:Meristem / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D008856:Microscopy, Fluorescence; D008969:Molecular Sequence Data; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D018517:Plant Roots / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D018547:Plant Stems / Q000235:genetics / Q000378:metabolism / Q000502:physiology; D030821:Plants, Genetically Modified; D011485:Protein Binding; D012689:Sequence Homology, Nucleic Acid; D020798:Two-Hybrid System Techniques; D014587:Ustilaginales / Q000235:genetics* / Q000378:metabolism / Q000502:physiology; D003313:Zea mays / Q000235:genetics* / Q000382:microbiology / Q000502:physiology
D005656:Fungal Proteins; D007210:Indoleacetic Acids; D008164:Luminescent Proteins; D010940:Plant Proteins