Adaptive regulation of miRNAs/milRNAs in tissue-specific interaction between apple and Valsa mali

Chengyu Gao , Binsen Zhao , Jian Zhang , Xuan Du , Jie Wang , Yan Guo , Yanting He , Hao Feng , Lili Huang

Horticulture Research ›› 2024, Vol. 11 ›› Issue (5) : 094

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Horticulture Research ›› 2024, Vol. 11 ›› Issue (5) :094 DOI: 10.1093/hr/uhae094
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Adaptive regulation of miRNAs/milRNAs in tissue-specific interaction between apple and Valsa mali
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Abstract

In plant-pathogen interactions, pathogens display tissue specificity, infecting and causing disease in particular tissues. However, the involvement of microRNAs/microRNA-like RNAs (miRNAs/milRNAs) in tissue-specific regulation during plant-pathogen interactions remains largely unexplored. This study investigates the differential expression of miRNAs/milRNAs, as well as their corresponding target genes, in interactions between Valsa mali (Vm) and different apple tissues. The results demonstrated that both apple miRNAs and Vm milRNAs exhibited distinct expression profiles when Vm infected bark and leaves, with functionally diverse corresponding target genes. Furthermore, one apple miRNA (Mdo-miR482a) and one Vm milRNA (Vm-milR57) were identified as exhibiting tissue-specific expression in interactions between Vm and apple bark or leaves. Mdo-miR482a was exclusively up-regulated in response to Vm infection in bark and target a nucleotide-binding leucine-rich repeat (NLR) gene of apple. When Mdo-miR482a was transiently over-expressed or silenced, the resistance was significantly reduced or improved. Similarly, transient expression of the NLR gene also showed an increase in resistance. Vm-milR57 could target two essential pathogenicity-related genes of Vm. During Vm infection in bark, the expression of Vm-milR57 was down-regulated to enhance the expression of the corresponding target gene to improve the pathogenicity. The study is the first to reveal tissue-specific characteristics of apple miRNAs and Vm milRNAs in interactions between Vm and different apple tissues, providing new insights into adaptive regulation in tissue-specific interactions between plants and fungi.

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Chengyu Gao, Binsen Zhao, Jian Zhang, Xuan Du, Jie Wang, Yan Guo, Yanting He, Hao Feng, Lili Huang. Adaptive regulation of miRNAs/milRNAs in tissue-specific interaction between apple and Valsa mali. Horticulture Research, 2024, 11 (5) : 094 DOI:10.1093/hr/uhae094

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Acknowledgements

This research was financially supported by the National Natural Science Foundation of China (U1903206, 32172375) and the Key Science and Technology Special Projects of Shaanxi Province (2020zdzx03-03-01). The authors would like to express their gratitude to Prof. Dongdong Niu at Nanjing Agricultural University for providing the pRS300 plasmid. The authors also extend their appreciation to Hua Zhao and Fengping Yuan from Northwest A&F University for their valuable assistance in optical microscopy. Lastly, the authors would like to acknowledge the anonymous reviewers and editors for their insightful comments, which greatly enhanced the quality of the manuscript.

Author contributions

L.H., H.F., and C.G. designed the study. C.G. analysed the data. B.Z., J.Z., X.D., J.W., Y.G., and Y.H. performed the experiments. C.G., H.F., and L.H. wrote the manuscript. All authors read and approved the final manuscript.

Data availability

All sRNA-Seq data have been deposited in the NCBI Sequence Read Archive under project number PRJNA987183. All degradome data have been deposited in the NCBI Sequence Read Archive under project number PRJNA987192.

All the scripts and pipelines used in this study have been archived in GitHub: https://github.com/GaoChengyu/tsDEMs.

Conflict of interest statement

The authors declare that they have no competing interests.

Supplementary data

Supplementary data is available at Horticulture Research online.

References

[1]

Barrett LG, Heil M. Unifying concepts and mechanisms in the specificity of plant-enemy interactions. Trends Plant Sci. 2012; 17: 282-92

[2]

Lacaze A, Joly DL. Structural specificity in plant-filamentous pathogen interactions. Mol Plant Pathol. 2020; 21: 1513-25

[3]

Fatima U, Senthil-Kumar M. Plant and pathogen nutrient acquisition strategies. Front Plant Sci. 2015; 6:750

[4]

Strugala R, Delventhal R, Schaffrath U. An organ-specific view on non-host resistance. Front Plant Sci. 2015; 6:526

[5]

Chuberre C, Plancot B, Driouich A. et al. Plant immunity is compartmentalized and specialized in roots. Front Plant Sci. 2018; 9:1692

[6]

Le Fevre R, O’Boyle B, Moscou MJ. et al. Colonization of barley by the broad-host Hemibiotrophic pathogen Phytophthora palmivora uncovers a leaf development-dependent involvement of Mlo. MPMI. 2016; 29:385-95

[7]

Hermanns M, Slusarenko AJ, Schlaich NL. Organ-specificity in a plant disease is determined independently of R gene signaling. MolPlant-Microbe Interact. 2003; 16:752-9

[8]

Schilling L, Matei A, Redkar A. et al. Virulence of the maize smut Ustilago maydis is shaped by organ-specific effectors. Mol Plant Pathol. 2014; 15:780-9

[9]

Shi J, Zhou T, Chen Q. Exploring the expanding universe of small RNAs. Nat Cell Biol. 2022; 24:415-23

[10]

Czech B, Munafò M, Ciabrelli F. et al. piRNA-guided genome defense: from biogenesis to silencing. Annu Rev Genet. 2018; 52: 131-57

[11]

Chen X, Rechavi O. Plant and animal small RNA communications between cells and organisms. Nat Rev Mol Cell Biol. 2022; 23: 185-203

[12]

Hua C, Zhao J-H, Guo H-S. Trans-kingdom RNA silencing in plant-fungal pathogen interactions. Mol Plant. 2018; 11:235-44

[13]

Navarro L, Dunoyer P, Jay F. et al. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science. 2006; 312:436-9

[14]

Qiao L, Zheng L, Sheng C. et al. Rice siR109944 suppresses plant immunity to sheath blight and impacts multiple agronomic traits by affecting auxin homeostasis. Plant J. 2020; 102:948-64

[15]

Vetukuri RR, Åsman AKM, Tellgren-Roth C. et al. Evidence for small RNAs homologous to effector-encoding genes and transposable elements in the oomycete Phytophthora infestans. PLoS One. 2012; 7:e51399

[16]

Fahlgren N, Bollmann SR, Kasschau KD. et al. Phytophthora have distinct endogenous small RNA populations that include short interfering and microRNAs. PLoS One. 2013; 8:e77181

[17]

Li M, Xie L, Wang M. et al. FoQDE2-dependent milRNA promotes Fusarium oxysporum f. sp. cubense virulence by silencing a glycosyl hydrolase coding gene expression. PLoS Pathog. 2022; 18:e1010157

[18]

Cai Q, Qiao L, Wang M. et al. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science. 2018; 360:1126-9

[19]

Wang B, Sun Y, Song N. et al. Puccinia striiformis f.sp. tritici microRNA-like RNA 1 (Pst-milR1), an important pathogenicity factor of Pst, impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene. New Phytol. 2017; 215:338-50

[20]

Xu L, Hu Y, Cao Y. et al. An expression atlas of miRNAs in Arabidopsis thaliana. Sci China Life Sci. 2018; 61:178-89

[21]

Devers EA, Branscheid A, May P. et al. Stars and symbiosis: microRNA- and microRNA∗-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 2011; 156:1990-2010

[22]

Meng Y, Shao C, Ma X. et al. Expression-based functional investigation of the organ-specific microRNAs in Arabidopsis. PLoS One. 2012; 7:e50870

[23]

Xu Y, Zhang T, Li Y. et al. Integrated analysis of large-scale omics data revealed relationship between tissue specificity and evolutionary dynamics of small RNAs in maize (Zea mays). Front Genet. 2020; 11:51

[24]

Wang S, Li P, Zhang J. et al. Generation of a high resolution map of sRNAs from Fusarium graminearum and analysis of responses to viral infection. Sci Rep. 2016; 6:26151

[25]

Lau AYT, Xie Y, Cheung MK. et al. Genome-wide mRNA and miRNA analysis in the early stages of germ tube outgrowth in Coprinopsis cinerea. Fungal Genet Biol. 2020; 142:103416

[26]

Jin Y, Zhao J-H, Zhao P. et al. A fungal milRNA mediates epigenetic repression of a virulence gene in Verticillium dahliae. Philos Trans R Soc Lond Ser B Biol Sci. 2019; 374:20180309

[27]

Wang X, Zang R, Yin Z. et al. Delimiting cryptic pathogen species causing apple Valsa canker with multilocus data. Ecol Evol. 2014; 4:1369-80

[28]

Abe K, Kotoda N, Kato H. et al. Resistance sources to Valsa canker (Valsa ceratosperma) in a germplasm collection of diverse Malus species. Plant Breed. 2007; 126:449-53

[29]

Yin Z, Ke X, Li Z. et al. Unconventional recombination in the mating type locus of heterothallic apple canker pathogen Valsa mali. G3 GenesGenomesGenetics. 2017; 7:1259-65

[30]

Ke X, Huang L, Han Q. et al. Histological and cytological investigations of the infection and colonization of apple bark by Valsa mali var. mali. Australas. Plant Pathol. 2013; 42:85-93

[31]

Xu M, Li G, Guo Y. et al. A fungal microRNA-like RNA subverts host immunity and facilitates pathogen infection by silencing two host receptor-like kinase genes. New Phytol. 2022; 233: 2503-19

[32]

Guo Z, Kuang Z, Zhao Y. et al. PmiREN2.0: from data annotation to functional exploration of plant microRNAs. Nucleic Acids Res. 2022; 50:D1475-82

[33]

Yu Y, Jia T, Chen X. The ‘how’ and ‘where’ of plant microRNAs. New Phytol. 2017; 216:1002-17

[34]

Rajagopalan R, Vaucheret H, Trejo J. et al. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 2006; 20:3407-25

[35]

Wang J, Chen T, Han M. et al. Plant NLR immune receptor Tm-22 activation requires NB-ARC domain-mediated self-association of CC domain. PLoS Pathog. 2020; 16:e1008475

[36]

Laflamme B, Dillon MM, Martel A. et al. The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science. 2020; 367:763-8

[37]

Xu M, Guo Y, Tian R. et al. Adaptive regulation of virulence genes by microRNA-like RNAs in Valsa mali. New Phytol. 2020; 227: 899-913

[38]

Abe H, Urao T, Ito T. et al. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell. 2003; 15:63-78

[39]

Allen A, Islamovic E, Kaur J. et al. Transgenic maize plants expressing the Totivirus antifungal protein, KP4, are highly resistant to corn smut. Plant Biotechnol J. 2011; 9:857-64

[40]

Koroban NV, Kudryavtseva AV, Krasnov GS. et al. The role of microRNA in abiotic stress response in plants. Mol Biol (Mosk). 2016; 50:337-43

[41]

Huang C-Y, Wang H, Hu P. et al. Small RNAs - big players in plant-microbe interactions. Cell Host Microbe. 2019; 26:173-82

[42]

Shahid S, Kim G, Johnson NR. et al. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature. 2018; 553:82-5

[43]

Lu S, Sun Y-H, Shi R. et al. Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell. 2005; 17:2186-203

[44]

Ma W, Chen C, Liu Y. et al. Coupling of microRNA-directed phased small interfering RNA generation from long noncoding genes with alternative splicing and alternative polyadenylation in small RNA-mediated gene silencing. New Phytol. 2018; 217: 1535-50

[45]

Zhai J, Jeong D-H, De Paoli E. et al. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 2011; 25:2540-53

[46]

Shivaprasad PV, Chen H-M, Patel K. et al. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell. 2012; 24:859-74

[47]

Wu C-H, Abd-El-Haliem A, Bozkurt TO. et al. NLR network mediates immunity to diverse plant pathogens. Proc Natl Acad Sci USA. 2017; 114:8113-8

[48]

Canto-Pastor A, Santos BAMC, Valli AA. et al. Enhanced resistance to bacterial and oomycete pathogens by short tandem target mimic RNAs in tomato. Proc Natl Acad Sci USA. 2019; 116: 2755-60

[49]

Liu J, Osbourn A, Ma P. MYB transcription factors as regulators of Phenylpropanoid metabolism in plants. Mol Plant. 2015; 8: 689-708

[50]

Cao S, Li W, Li C. et al. The CHY-type zinc finger protein FgChy1 regulates polarized growth, pathogenicity, and microtubule assembly in Fusarium graminearum. MPMI. 2021; 34: 362-75

[51]

Aliyu SR, Lin L, Chen X. et al. Disruption of putative short-chain acyl-CoA dehydrogenases compromised free radical scavenging, conidiogenesis, and pathogenesis of Magnaporthe oryzae. Exp Mycol. 2019; 127:23-34

[52]

Daccord N, Celton J-M, Linsmith G. et al. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nat Genet. 2017; 49:1099-106

[53]

Yin Z, Liu H, Li Z. et al. Genome sequence of Valsa canker pathogens uncovers a potential adaptation of colonization of woody bark. New Phytol. 2015; 208:1202-16

[54]

Dai X, Zhuang Z, Zhao PX. psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res. 2018; 46: W49-54

[55]

Chen C, Wu Y, Li J. et al. TBtools-II: a ‘one for all, all for one’ bioinformatics platform for biological big-data mining. Mol Plant. 2023; 16:1733-42

[56]

Jumper J, Evans R, Pritzel A. et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021; 596:583-9

[57]

Camacho C, Coulouris G, Avagyan V. et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009; 10:421

[58]

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004; 32: 1792-7

[59]

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinforma Oxf Engl. 2009; 25:1972-3

[60]

Minh BQ, Schmidt HA, Chernomor O. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020; 37:1530-4

[61]

Yu G. Using ggtree to visualize data on tree-like structures. Current Protocols. 2020; 69:e96

[62]

Varkonyi-Gasic E, Wu R, Wood M. et al. Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods. 2007; 3:12

[63]

Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3:1101-8

[64]

Zhou X, Li G, Xu J-R. Efficient approaches for generating GFP fusion and epitope-tagging constructs in filamentous fungi. Methods Mol Biol Clifton NJ. 2011; 722:199-212

[65]

Wang Y, Wang Z, Yang W. et al. Degradation of fungal MicroRNAs triggered by short tandem target mimics is via the small-RNA-degrading nuclease. Appl Environ Microbiol. 2019; 85: e03132-18

[66]

Gao J, Li Y, Ke X. et al. Development of genetic transformation system of Valsa mali of apple mediated by PEG. Wei Sheng Wu Xue Bao. 2011; 51:1194-9

[67]

Xu M, Gao X, Chen J. et al. The feruloyl esterase genes are required for full pathogenicity of the apple tree canker pathogen Valsa mali. Mol Plant Pathol. 2018; 19:1353-63

[68]

Feng H, Xu M, Gao Y. et al. Vm-milR37 contributes to pathogenicity by regulating glutathione peroxidase gene VmGP in Valsa mali. Mol Plant Pathol. 2021; 22:243-54

[69]

Zhang Q, Ma C, Zhang Y. et al. A single-nucleotide polymorphism in the promoter of a hairpin RNA contributes to Alternaria alternata leaf spot resistance in apple (Malus × domestica). Plant Cell. 2018; 30:1924-42

[70]

Dai H, Li W, Han G. et al. Development of a seedling clone with high regeneration capacity and susceptibility to agrobacterium in apple. Sci Hortic. 2013; 164:202-8

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