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Long noncoding RNAs involve in resistance to Verticillium dahliae, a fungal disease in cotton.

ABSTRACT: Long noncoding RNAs (lncRNAs) have several known functions in plant development, but their possible roles in responding to plant disease remain largely unresolved. In this study, we described a comprehensive disease-responding lncRNA profiles in defence against a cotton fungal disease Verticillium dahliae. We further revealed the conserved and specific characters of disease-responding process between two cotton species. Conservatively for two cotton species, we found the expression dominance of induced lncRNAs in the Dt subgenome, indicating a biased induction pattern in the co-existing subgenomes of allotetraploid cotton. Comparative analysis of lncRNA expression and their proposed functions in resistant Gossypium barbadense cv. '7124' versus susceptible Gossypium hirsutum cv. 'YZ1' revealed their distinct disease response mechanisms. Species-specific (LS) lncRNAs containing more SNPs displayed a fiercer inducing level postinfection than the species-conserved (core) lncRNAs. Gene Ontology enrichment of LS lncRNAs and core lncRNAs indicates distinct roles in the process of biotic stimulus. Further functional analysis showed that two core lncRNAs, GhlncNAT-ANX2- and GhlncNAT-RLP7-silenced seedlings, displayed an enhanced resistance towards V. dahliae and Botrytis cinerea, possibly associated with the increased expression of LOX1 and LOX2. This study represents the first characterization of lncRNAs involved in resistance to fungal disease and provides new clues to elucidate cotton disease response mechanism.

SUBMITTER: Zhang L

PROVIDER: S-EPMC5978870 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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Long noncoding RNAs involve in resistance to Verticillium dahliae, a fungal disease in cotton.

Zhang Lin L Wang Maojun M Li Nannan N Wang Honglei H Qiu Ping P Pei Liuling L Xu Zheng Z Wang Tianyi T Gao Erlin E Liu Junxia J Liu Shiming S Hu Qin Q Miao Yuhuan Y Lindsey Keith K Tu Lili L Zhu Longfu L Zhang Xianlong X

Plant biotechnology journal 20171221 6

Long noncoding RNAs (lncRNAs) have several known functions in plant development, but their possible roles in responding to plant disease remain largely unresolved. In this study, we described a comprehensive disease-responding lncRNA profiles in defence against a cotton fungal disease Verticillium dahliae. We further revealed the conserved and specific characters of disease-responding process between two cotton species. Conservatively for two cotton species, we found the expression dominance of ...[more]

PMID: 29149461

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Project description:Long intergenic non-coding RNAs (lincRNAs) have been demonstrated to be vital regulators of diverse biological processes in both animals and plants. While many lincRNAs have been identified in cotton, we still know little about the repositories and conservativeness of lincRNAs in different cotton species or about their role in responding to biotic stresses. Here, by using publicly available RNA-seq datasets from diverse sources, including experiments of Verticillium dahliae (Vd) infection, we identified 24,425 and 17,713 lincRNAs, respectively, in Gossypium hirsutum (Ghr) and G. barbadense (Gba), the two cultivated allotetraploid cotton species, and 6933 and 5911 lincRNAs, respectively, in G. arboreum (Gar) and G. raimondii (Gra), the two extant diploid progenitors of the allotetraploid cotton. While closely related subgenomes, such as Ghr_At and Gba_At, tend to have more conserved lincRNAs, most lincRNAs are species-specific. The majority of the synthetic and transcribed lincRNAs (78.2%) have a one-to-one orthologous relationship between different (sub)genomes, although a few of them (0.7%) are retained in all (sub)genomes of the four species. The Vd responsiveness of lincRNAs seems to be positively associated with their conservation level. The major functionalities of the Vd-responsive lincRNAs seem to be largely conserved amongst Gra, Ghr, and Gba. Many Vd-responsive Ghr-lincRNAs overlap with Vd-responsive QTL, and several lincRNAs were predicted to be endogenous target mimicries of miR482/2118, with a pair being highly conserved between Ghr and Gba. On top of the confirmation of the feature characteristics of the lincRNAs previously reported in cotton and other species, our study provided new insights into the conservativeness and divergence of lincRNAs during cotton evolution and into the relationship between the conservativeness and Vd responsiveness of lincRNAs. The study also identified candidate lincRNAs with a potential role in disease response for functional characterization.

Project description:Verticillium wilt, mainly caused by a soil-inhabiting fungus Verticillium dahliae, can seriously reduce the yield and quality of cotton. The complex mechanism underlying cotton resistance to Verticillium wilt remains largely unknown. In plants, reactive oxygen species (ROS) mediated by Rbohs is one of the earliest responses of plants to biotic and abiotic stresses. In our previous study, we performed a time-course phospho-proteomic analysis of roots of resistant and susceptible cotton varieties in response to V. dahliae, and found early differentially expressed protein burst oxidase homolog protein D (GhRbohD). However, the role of GhRbohD-mediated ROS in cotton defense against V. dahliae needs further investigation. In this study, we analyzed the function of GhRbohD-mediated resistance of cotton against V. dahliae in vitro and in vivo. Bioinformatics analysis showed that GhRbohD possessed the conservative structural attributes of Rbohs family, 12 members of RbohD out of 57 Rbohs in cotton. The expression of GhRbohD was significantly upregulated after V. dahliae inoculation, peaking at 6 hpi, and the phosphorylation level was also increased. A VIGS test demonstrated that ROS production, NO, H2O2 and Ca2+ contents of GhRbohD-silenced cotton plants were significantly reduced, and lignin synthesis and callose accumulation were damaged, important reasons for the impairment of GhRbohD-silenced cotton's defense against V. dahliae. The expression levels of resistance-related genes were downregulated in GhRbohD-silenced cotton by qRT-PCR, mainly involving the lignin metabolism pathway and the jasmonic acid signaling pathway. However, overexpression of GhRbohD enhanced resistance of transgenic Arabidopsis to V. dahliae challenge. Furthermore, Y2H assays were applied to find that GhPBL9 and GhRPL12C may interact with GhRbohD. These results strongly support that GhRbohD activates ROS production to positively regulate the resistance of plants against V. dahliae.

Project description:BackgroundThe extracellular space between the cell wall and plasma membrane is a battlefield in plant-pathogen interactions. Within this space, the pathogen employs its secretome to attack the host in a variety of ways, including immunity manipulation. However, the role of the plant secretome is rarely studied for its role in disease resistance.ResultsHere, we examined the secretome of Verticillium wilt-resistant Gossypium hirsutum cultivar Zhongzhimian No.2 (ZZM2, encoding 95,327 predicted coding sequences) to determine its role in disease resistance against the wilt causal agent, Verticillium dahliae. Bioinformatics-driven analyses showed that the ZZM2 genome encodes 2085 secreted proteins and that these display disequilibrium in their distribution among the chromosomes. The cotton secretome displayed differences in the abundance of certain amino acid residues as compared to the remaining encoded proteins due to the localization of these putative proteins in the extracellular space. The secretome analysis revealed conservation for an allotetraploid genome, which nevertheless exhibited variation among orthologs and comparable unique genes between the two sub-genomes. Secretome annotation strongly suggested its involvement in extracellular stress responses (hydrolase activity, oxidoreductase activity, and extracellular region, etc.), thus contributing to resistance against the V. dahliae infection. Furthermore, the defense response genes (immunity marker NbHIN1, salicylic acid marker NbPR1, and jasmonic acid marker NbLOX4) were activated to varying degrees when Nicotina benthamiana leaves were agro-infiltrated with 28 randomly selected members, suggesting that the secretome plays an important role in the immunity response. Finally, gene silencing assays of 11 members from 13 selected candidates in ZZM2 displayed higher susceptibility to V. dahliae, suggesting that the secretome members confer the Verticillium wilt resistance in cotton.ConclusionsOur data demonstrate that the cotton secretome plays an important role in Verticillium wilt resistance, facilitating the development of the resistance gene markers and increasing the understanding of the mechanisms regulating disease resistance.

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Long noncoding RNAs involve in resistance to Verticillium dahliae, a fungal disease in cotton.

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Long noncoding RNAs involve in resistance to Verticillium dahliae, a fungal disease in cotton.

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