SUPPRESSOR OF APICAL DOMINANCE 1 of Sporisorium reilianum Modulates Inflorescence Branching Architecture in Maize and Arabidopsis

Abstract

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.

SUPPRESSOR OF APICAL DOMINANCE1 of Sporisorium reilianum changes inflorescence branching at early stages in di- and monocot plants and induces fruit abortion in Arabidopsis thaliana

“…These A. thaliana plants were bushier after eight weeks of growth due to increased secondary branching. 6 This demonstrated that GFP-SAD1 is able to affect the inflorescence branching pattern of transgenic A. thaliana without the aid of other fungal proteins. Here we present evaluations of time course experiments in S. reilianum-infected maize and transgenic A. thaliana plants in order to study the temporal dynamics of developmental changes.…”

“…Analysis of maize plants that were infected by S. reilianum, lacking or expressing SAD1, indicated that SAD1, even though expressed in every colonized plant tissue, 6 has an effect only on female inflorescences. At the female inflorescence, SAD1 manipulates bud outgrowth and induces growth of subapical ears.…”

“…At the female inflorescence, SAD1 manipulates bud outgrowth and induces growth of subapical ears. 6 The process of branching is controlled by many environmental and endogenous factors. 7 Hormones like auxin and strigolactones are main players in control of bud outgrowth.…”

“…5 Recently, we found that the S. reilianum effector SUPPRES-SOR OF APICAL DOMINANCE1 (SAD1) is the causal agent of the induction of subapical ears in S. reilianum-infected maize plants. 6 We generated homozygous transgenic A. thaliana plants expressing P 35S :GFP-SAD1 (At_GFP-SAD1). These A. thaliana plants were bushier after eight weeks of growth due to increased secondary branching.…”

Smut infection of perennial hosts: the genome and the transcriptome of the Brassicaceae smut fungus Thecaphora thlaspeos reveal functionally conserved and novel effectors

“…Subsequently, fungal hyphae proliferate inside the apoplast and/or grow through host cells, establishing an intimate contact zone for the exchange of nutrients and proteins. Functional genomic analyses of the grass smut fungi U. maydis, Sporisorium reilianum and U. hordei have greatly contributed to our understanding of smut infection and the associated host responses (K€ amper et al, 2006;Brefort et al, 2009;Ghareeb et al, 2015;Lanver et al, 2018). In short, these studies have revealed different repertoires of conserved and host-adapted effector proteins (Okmen & Doehlemann, 2014;Lanver et al, 2017).…”