Transcriptome Analysis Reveals Contrasting Plant Responses of Sorghum bicolor upon Colonization by Two Formae Speciales of Sporisorium reilianum

Abstract

The biotrophic fungus Sporisorium reilianum exists in two host-adapted formae speciales that cause head smut in maize (S. reilianum f. sp. zeae; SRZ) and sorghum (S. reilianum f. sp. reilianum; SRS). In sorghum, the spread of SRZ is limited to the leaves. To understand the plant responses to each forma specialis, we determined the transcriptome of sorghum leaves inoculated either with SRS or SRZ. Fungal inoculation led to gene expression rather than suppression in sorghum. SRZ induced a much greater number of genes than SRS. Each forma specialis induced a distinct set of plant genes. The SRZ-induced genes were involved in plant defense mainly at the plasma membrane and were associated with the Molecular Function Gene Ontology terms chitin binding, abscisic acid binding, protein phosphatase inhibitor activity, terpene synthase activity, chitinase activity, transmembrane transporter activity and signaling receptor activity. Specifically, we found an upregulation of the genes involved in phospholipid degradation and sphingolipid biosynthesis, suggesting that the lipid content of the plant plasma membrane may contribute to preventing the systemic spread of SRZ. In contrast, the colonization of sorghum with SRS increased the expression of the genes involved in the detoxification of cellular oxidants and in the unfolded protein response at the endoplasmic reticulum, as well as of the genes modifying the cuticle wax and lipid composition through the generation of alkanes and phytosterols. These results identified plant compartments that may have a function in resistance against SRZ (plasma membrane) and susceptibility towards SRS (endoplasmic reticulum) that need more attention in the future.

Plant Responses of Maize to Two formae speciales of Sporisorium reilianum Support Recent Fungal Host Jump

“…This situation is very different from the plant responses that both fungal varieties cause on sorghum. On sorghum, SRZ causes expression of a plethora of different defense genes [18], which corresponds well to the strong plant response visual on SRZ-inoculated leaves at three to seven days post-inoculation [20]. In contrast, except for genes coping with the consequences of ROS accumulation, plants inoculated with SRS do not show induction of the SRZ-induced defense genes, suggesting that at 3 dpi, SRS successfully prevents upregulation of further defense responses.…”

“…The very efficient downregulation of early induced defense gene expression after penetration shows that the fungus is highly adapted to its host plant. Like U. maydis on maize, SRS on sorghum does not show defense gene expression at 3 dpi [18], suggesting a similar long-time adaptation. In contrast, SRS and SRZ cause comparable defense responses on maize, indicating that the time for host adaptation has been minimal so far.…”

“…Likewise, S. reilianum f. sp. reilianum does not show severe plant defense responses after successful host colonization [18], which suggests that SRS can downregulate initially induced defense responses of sorghum. This indicates that SRS is as well adapted to sorghum as U. maydis is to maize.…”

“…In contrast, the presence of S. reilianum f. sp. reilianum in sorghum led to upregulation of genes involved in detoxification of cellular oxidants, of genes involved in the unfolded protein response, and of genes potentially modifying the cuticle wax and lipid composition of the plant [18]. Here we complement this analysis by determining the plant response of maize seedling leaves to the same formae speciales of S. reilianum.…”

“…To better understand the plant processes involved in host selection of S. reilianum, we recently analyzed the plant responses of sorghum seedling leaves colonized by either one of the two formae speciales [18]. This analysis showed distinct plant responses to each forma specialis.…”