Auxin, Abscisic Acid and Jasmonate Are the Central Players in Rice Sheath Rot Caused by Sarocladium oryzae and Pseudomonas fuscovaginae

Abstract

Sheath rot is an emerging rice disease that causes severe yield losses worldwide. The main causal agents are the toxin producers Sarocladium oryzae and Pseudomonas fuscovaginae. The fungus S. oryzae produces helvolic acid and cerulenin and the bacterium P. fuscovaginae produces cyclic lipopeptides. Helvolic acid and the lipopeptide, fuscopeptin, inhibit membrane-bound H+-ATPase pumps in the rice plant. To manage rice sheath rot, a better understanding of the host response and virulence strategies of the pathogens is required. This study investigated the interaction of the sheath rot pathogens with their host and the role of their toxins herein. Japonica rice was inoculated with high- and low-helvolic acid-producing S. oryzae isolates or with P. fuscovaginae wild type and fuscopeptin mutant strains. During infection, cerulenin, helvolic acid and the phytohormones abscisic acid, jasmonate, auxin and salicylic acid were quantified in the sheath. In addition, disease severity and grain yield parameters were assessed. Rice plants responded to high-toxin-producing S. oryzae and P. fuscovaginae strains with an increase in abscisic acid, jasmonate and auxin levels. We conclude that, for both pathogens, toxins play a core role during sheath rot infection. S. oryzae and P. fuscovaginae interact with their host in a similar way. This may explain why both sheath rot pathogens cause very similar symptoms despite their different nature.

Metabolomic and Transcriptomic Changes Induced by Potassium Deficiency During Sarocladium oryzae Infection Reveal Insights into Rice Sheath Rot Disease Resistance

“…JA is initially synthesized from linolenic and linoleic acid. Thus, the hyperaccumulation of linoleic acid may suppress the JA level of the host plant, which is in agreement with a previous report that ShR infection slightly decreased the JA content of the host plant (Peeters et al 2020). In the present study, we only investigated the effects of K starvation on lipid metabolism and lipid peroxidation during S. oryzae infection; however, other nutrient deficiencies might also induce membrane peroxidation, and whether other nutrient deficiencies could also promote ShR development needs further study.…”

“…3). The content of indoleacetic acid (IAA) in the diseased tissues was up-regulated, which consistent with a previous study reported that S. oryzae infection triggered strong IAA responses and IAA levels positively correlated with the lesion area (Peeters et al 2020). Dihydrokaempferol is a derivative of flavonoids, the upregulation of which indicates that anthocyanin metabolism is activated.…”

“…Previous studies demonstrated that K deficiency promoted the biosynthesis of oxylipin (Troufflard et al 2010;Armengaud et al 2010). Furthermore, S. oryzae infection profoundly altered the hormone levels of the host plant, such as the content of abscisic and jasmonic acids (Peeters et al 2020). Notably, lipid metabolism provides a substrate for the biosynthesis of jasmonic acid and oxylipids (Conconi et al 1996;Torres-Franklin et al 2009).…”

CRISPR/Cas9-Mediated Gene Editing of Vacuolar ATPase Subunit D Mediates Phytohormone Biosynthesis and Virus Resistance in Rice

“…Transcriptomic analysis showed that Osv-ATPase d is involved in plant hormone mediation; thus, the plant hormones in editing line 5 and the wild type were then quanti ed by ultra-high-performance liquid chromatography-triple quadrupole mass spectrometry (UPLC-MS/MS) (Hu et al 2020;Peeters et al 2020). As expected, Osv-ATPase d was indeed involved in mediating plant hormone biosynthesis.…”

“…Eukaryotic v-ATPases are multiprotein complexes, and v-ATPase subunit d (v-ATPase d) is part of an integral, membraneembedded V0 complex (Hohlweg et al 2018). The pathogens Sarocladium oryzae and Pseudomonas fuscovaginae cause rice sheath rot and produce cyclic lipopeptides to inhibit membranebound H + -ATPase pumps in the rice plant, resulting in reduced abscisic acid (ABA), jasmonate acid (JA) and auxin levels and grain yield in rice (Peeters et al 2020). Plant hormones are pivotal for biotic and abiotic resistance, and rice hormones have diverse functions in rice resistance against different viruses (Xie et al 2018;Yan et al 2015;Zhang et al 2020).…”