Abstract

Temperature influences the physiological processes and ecology of both hosts and endophytes; however, it remains unclear how long noncoding RNAs (lncRNAs) modulate the consequences of temperature-dependent changes in host–pathogen interactions. To explore the role of lncRNAs in culm gall formation induced by the smut fungus Ustilago esculenta in Zizania latifolia, we employed RNA sequencing to identify lncRNAs and their potential cis-targets in Z. latifolia and U. esculenta under different temperatures. In Z. latifolia and U. esculenta, we identified 3194 and 173 lncRNAs as well as 126 and four potential target genes for differentially expressed lncRNAs, respectively. Further function and expression analysis revealed that lncRNA ZlMSTRG.11348 regulates amino acid metabolism in Z. latifolia and lncRNA UeMSTRG.02678 regulates amino acid transport in U. esculenta. The plant defence response was also found to be regulated by lncRNAs and suppressed in Z. latifolia infected with U. esculenta grown at 25 °C, which may result from the expression of effector genes in U. esculenta. Moreover, in Z. latifolia infected with U. esculenta, the expression of genes related to phytohormones was altered under different temperatures. Our results demonstrate that lncRNAs are important components of the regulatory networks in plant-microbe-environment interactions, and may play a part in regulating culm swelling in Z. latifolia plants.

Highlights

  • The smut fungus Ustilago esculenta infects the host Zizania latifolia plant causing formation of culm gall [1,2,3]

  • The other plants, including Z. latifolia plants without U. esculenta infection (CK) grown at 25 ◦ C (CK25), as well as CK and JB plants grown at 35 ◦ C (CK35, JB35), did not produce swollen culm gall, and exhibited a significant decrease in length, weight, perimeter, and volume in culms compared to JB25 (p < 0.05)

  • These results clearly demonstrate that culm gall can form in JB plants grown at 25 ◦ C, while gall induction was completely suppressed by a temperature of 35 ◦ C

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Summary

Introduction

The smut fungus Ustilago esculenta infects the host Zizania latifolia plant causing formation of culm gall [1,2,3]. Apart from culm hypertrophy, which represents the characteristic symptom associated with infection of this fungus, no apparent change appears in Z. latifolia plants [2]. U. esculenta completes its life cycle in plant tissues, leading to formation of culm gall [3,7]. In terms of the ‘disease triangle,’ disease outbreaks occur only under proper environmental conditions following pathogen colonisation and proliferation in host plants. Temperature, which generally influences the physiology, ecology, and growth of hosts and microorganisms, is considered to be integral to the promotion of disease outbreaks in plants [8]

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