Copper microRNAs modulate the formation of giant feeding cells induced by the root knot nematode Meloidogyne incognita in Arabidopsis thaliana.
Arabidopsis
copper
microRNAs
root-knot nematodes
signalling
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
received:
17
11
2021
accepted:
10
06
2022
pubmed:
9
7
2022
medline:
11
9
2022
entrez:
8
7
2022
Statut:
ppublish
Résumé
Root-knot nematodes (RKNs) are root endoparasites that induce the dedifferentiation of a few root cells and the reprogramming of their gene expression to generate giant hypermetabolic feeding cells. We identified two microRNA families, miR408 and miR398, as upregulated in Arabidopsis thaliana and Solanum lycopersicum roots infected by RKNs. In plants, the expression of these two conserved microRNA families is known to be activated by the SPL7 transcription factor in response to copper starvation. By combining functional approaches, we deciphered the network involving these microRNAs, their regulator and their targets. MIR408 expression was located within nematode-induced feeding cells like its regulator SPL7 and was regulated by copper. Moreover, infection assays with mir408 and spl7 knockout mutants or lines expressing targets rendered resistant to cleavage by miR398 demonstrated the essential role of the SPL7/MIR408/MIR398 module in the formation of giant feeding cells. Our findings reveal how perturbation of plant copper homeostasis, via the SPL7/MIR408/MIR398 module, modulates the development of nematode-induced feeding cells.
Substances chimiques
Arabidopsis Proteins
0
DNA-Binding Proteins
0
MicroRNAs
0
SPL7 protein, Arabidopsis
0
Transcription Factors
0
Copper
789U1901C5
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
283-295Informations de copyright
© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.
Références
Abad P, Williamson VM. 2010. Plant nematode interaction: a sophisticated dialogue. Advances in Botanical Research 53: 147-192.
de Almeida Engler J, Gheysen G. 2013. Nematode-induced endoreduplication in plant host cells: why and how? Molecular Plant-Microbe Interactions 26: 17-24.
Araki R, Mermod M, Yamasaki H, Kamiya T, Fujiwara T, Shikanai T. 2018. SPL7 locally regulates copper-homeostasis-related genes in Arabidopsis. Journal of Plant Physiology 224-225: 137-143.
Axtell MJ. 2013. Classification and comparison of small RNAs from plants. Annual Review of Plant Biology 64: 137-159.
Barciszewska-Pacak M, Milanowska K, Knop K, Bielewicz D, Nuc P, Plewka P, Pacak AM, Vazquez F, Karlowski W, Jarmolowski A et al. 2015. Arabidopsis microRNA expression regulation in a wide range of abiotic stress responses. Frontiers in Plant Science 6: 410.
Bartlem DG, Jones MGK, Hammes UZ. 2014. Vascularization and nutrient delivery at root-knot nematode feeding sites in host roots. Journal of Experimental Botany 65: 1789-1798.
Beauclair L, Yu A, Bouché N. 2010. MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. The Plant Journal 62: 454-462.
Bernal M, Casero D, Singh V, Wilson GT, Grande A, Yang H, Dodani SC, Pellegrini M, Huijser P, Connolly EL et al. 2012. Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24: 738-761.
Blok VC, Jones JT, Phillips MS, Trudgill DL. 2008. Parasitism genes and host range disparities in biotrophic nematodes: the conundrum of polyphagy versus specialisation. BioEssays 30: 249-259.
Brousse C, Liu Q, Beauclair L, Deremetz A, Axtell MJ, Bouché N. 2014. A non-canonical plant microRNA target site. Nucleic Acids Research 42: 5270-5279.
Burkhead JL, Gogolin Reynolds KA, Abdel-Ghany SE, Cohu CM, Pilon M. 2009. Copper homeostasis. New Phytologist 182: 799-816.
Cabrera J, Barcala M, García A, Rio-Machín A, Medina C, Jaubert-Possamai S, Favery B, Maizel A, Ruiz-Ferrer V, Fenoll C et al. 2016. Differentially expressed small RNAs in Arabidopsis galls formed by Meloidogyne javanica: a functional role for miR390 and its TAS3-derived tasiRNAs. New Phytologist 209: 1625-1640.
Cabrera J, Bustos R, Favery B, Fenoll C, Escobar C. 2014. NEMATIC: a simple and versatile tool for the insilico analysis of plant-nematode interactions. Molecular Plant Pathology 15: 627-636.
Cabrera J, Olmo R, Ruiz-Ferrer V, Abreu I, Hermans C, Martinez-Argudo I, Fenoll C, Escobar C. 2018. A phenotyping method of giant cells from root-knot nematode feeding sites by confocal microscopy highlights a role for CHITINASE-LIKE 1 in Arabidopsis. International Journal of Molecular Sciences 19: 429.
Cai Q, Qiao L, Wang M, He B, Lin F-M, Palmquist J, Huang S-D, Jin H. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360: 1126-1129.
Caillaud M-C, Favery B. 2016. In vivo imaging of microtubule organization in dividing giant cell. Methods in Molecular Biology 1370: 137-144.
Caillaud M-C, Lecomte P, Jammes F, Quentin M, Pagnotta S, Andrio E, de Almeida EJ, Marfaing N, Gounon P, Abad P et al. 2008. MAP65-3 microtubule-associated protein is essential for nematode-induced giant cell ontogenesis in Arabidopsis. Plant Cell 20: 423-437.
Chávez Montes RA, De Fátima R-CF, De Paoli E, Accerbi M, Rymarquis LA, Mahalingam G, Marsch-Martínez N, Meyers BC, Green PJ, De Folter S. 2014. Sample sequencing of vascular plants demonstrates widespread conservation and divergence of microRNAs. Nature Communications 5: 3722.
Curaba J, Singh MB, Bhalla PL. 2014. miRNAs in the crosstalk between phytohormone signalling pathways. Journal of Experimental Botany 65: 1425-1438.
Dai X, Zhuang Z, Zhao PX. 2018. PsRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Research 46: W49-W54.
Díaz-Manzano FE, Cabrera J, Ripoll J-JJ, Del Olmo I, Andrés MF, Silva AC, Barcala M, Sánchez M, Ruíz-Ferrer V, de Almeida-Engler J et al. 2018. A role for the gene regulatory module microRNA172/TARGET OF EARLY ACTIVATION TAGGED 1/FLOWERING LOCUS T (miRNA172/TOE1/FT) in the feeding sites induced by Meloidogyne javanica in Arabidopsis thaliana. New Phytologist 217: 813-827.
Dunker F, Trutzenberg A, Rothenpieler JS, Kuhn S, Pröls R, Schreiber T, Tissier A, Kemen A, Kemen E, Hückelhoven R et al. 2020. Oomycete small RNAs bind to the plant RNA-induced silencing complex for virulence. eLife 9: e56096.
Ediz SA, Dickerson OJ. 1976. Life cycle, pathogenicity, histopathology, and host range of race 5 of the barley root-knot nematode. Journal of Nematology 8: 228-231.
Escobar C, Brown S, Mitchum MG. 2011. Transcriptomic and proteomic analysis of the plant response to nematode infection. In: Jones J, Gheysen G, Fenoll C, eds. Genomics and molecular genetics of plant-nematode interactions. Dordrecht, the Netherlands: Springer, 157-173.
Favery B, Dubreuil G, Chen M-S, Giron D, Abad P. 2020. Gall-inducing parasites: convergent and conserved strategies of plant manipulation by insects and nematodes. Annual Review of Phytopathology 58: 1-22.
Favery B, Lecomte P, Gil N, Bechtold N, Bouchez D, Dalmasso A, Abad P. 1998. RPE, a plant gene involved in early developmental steps of nematode feeding cells. EMBO Journal 17: 6799-6811.
Fu Y, Mason AS, Zhang Y, Lin B, Xiao M, Fu D, Yu H. 2019. MicroRNA-mRNA expression profiles and their potential role in cadmium stress response in Brassica napus. BMC Plant Biology 19: 570.
Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ. 2007. miRBase: tools for microRNA genomics. Nucleic Acids Research 36: D154-D158.
Hoang NT, Tóth K, Stacey G. 2020. The role of microRNAs in the legume-Rhizobium nitrogen-fixing symbiosis. Journal of Experimental Botany 71: 1668-1680.
Holbein J, Franke RB, Marhavý P, Fujita S, Górecka M, Sobczak M, Geldner N, Schreiber L, Grundler FMW, Siddique S. 2019. Root endodermal barrier system contributes to defence against plant-parasitic cyst and root-knot nematodes. The Plant Journal 100: 221-236.
Hutvágner G, McLachlan J, Pasquinelli AE, Bálint É, Tuschl T, Zamore PD. 2001. A cellular function for the RNA-interference enzyme dicer in the maturation of the let-7 small temporal RNA. Science 293: 834-838.
Jammes F, Lecomte P, Almeida-Engler J, Bitton F, Martin-Magniette M-LL, Renou JP, Abad P, Favery B, De Almeida-Engler J, Bitton F et al. 2005. Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsisa. The Plant Journal 44: 447-458.
Jaubert-Possamai S, Noureddine Y, Favery B. 2019. MicroRNAs, new players in the plant-nematode interaction. Frontiers in Plant Science 10: 1-8.
Jiang A, Guo Z, Pan J, Yang Y, Zhuang Y, Zuo D, Hao C, Gao Z, Xin P, Chu J et al. 2021. The PIF1-miR408-PLANTACYANIN repression cascade regulates light-dependent seed germination. Plant Cell 33: 1506-1529.
Kuo Y-W, Lin J-S, Li Y-C, Jhu M-Y, King Y-C, Jeng S-T. 2019. MicroR408 regulates defense response upon wounding in sweet potato. Journal of Experimental Botany 70: 469-483.
Li C, Zhang B. 2016. MicroRNAs in control of plant development. Journal of Cellular Physiology 231: 303-313.
Lobna H, Aymen EM, Hajer R, Naima M-B, Najet H-R. 2017. Biochemical and plant nutrient alterations induced by Meloidogyne javanica and Fusarium oxysporum f.sp.radicis lycopersici co-infection on tomato cultivars with differing level of resistance to M. javanica. European Journal of Plant Pathology 148: 463-472.
Ma C, Burd S, Lers A. 2015. miR408 is involved in abiotic stress responses in Arabidopsis. The Plant Journal 84: 169-187.
Maunoury N, Vaucheret H. 2011. AGO1 and AGO2 Act redundantly in miR408-mediated plantacyanin regulation. PLoS ONE 6: e28729.
Medina C, da Rocha M, Magliano M, Ratpopoulo A, Revel B, Marteu N, Magnone V, Lebrigand K, Cabrera J, Barcala M et al. 2017. Characterization of microRNAs from Arabidopsis galls highlights a role for miR159 in the plant response to the root-knot nematode Meloidogyne incognita. New Phytologist 216: 882-896.
Nguyen C-N, Perfus-Barbeoch L, Quentin M, Zhao J, Magliano M, Marteu N, Da Rocha M, Nottet N, Abad P, Favery B. 2018. A root-knot nematode small glycine and cysteine-rich secreted effector, MiSGCR1, is involved in plant parasitism. New Phytologist 217: 687-699.
Rancurel C, van Tran T, Elie C, Hilliou F. 2019. SATQPCR: website for statistical analysis of real-time quantitative PCR data. Molecular and Cellular Probes 46: 101418.
Reyt G, Chao Z, Flis P, Salas-González I, Castrillo G, Chao D-YY, Salt DE. 2020. Uclacyanin proteins are required for lignified nanodomain formation within casparian strips. Current Biology 30: 4103-4111.
Rodiuc N, Barlet X, Hok S, Perfus-Barbeoch L, Allasia V, Engler G, Séassau A, Marteu N, de Almeida-Engler J, Panabières F et al. 2016. Evolutionarily distant pathogens require the Arabidopsis phytosulfokine signalling pathway to establish disease. Plant, Cell & Environment 39: 1396-1407.
Schulman BRM, Esquela-Kerscher A, Slack FJ. 2005. Reciprocal expression of lin-41 and the microRNAs let-7 and mir-125 during mouse embryogenesis. Developmental Dynamics 234: 1046-1054.
Schulten A, Bytomski L, Quintana J, Bernal M, Krämer U. 2019. Do Arabidopsis squamosa promoter binding protein-like genes act together in plant acclimation to copper or zinc deficiency? Plant Direct 3: 590182.
Sommer F, Kropat J, Malasarn D, Grossoehme NE, Chen X, Giedroc DP, Merchant SS. 2011. The CRR1 nutritional copper sensor in chlamydomonas contains two distinct metal-responsive domains. Plant Cell 22: 4098-4113.
Thatcher SR, Burd S, Wright C, Lers A, Green PJ. 2015. Differential expression of miRNAs and their target genes in senescing leaves and siliques: insights from deep sequencing of small RNAs and cleaved target RNAs. Plant, Cell & Environment 38: 188-200.
Thomson JM, Newman M, Parker JS, Morin-Kensicki EM, Wright T, Hammond SM. 2006. Extensive post-transcriptional regulation of microRNAs and its implications for cancer. Genes and Development 20: 2202-2207.
Weiberg A, Jin H. 2015. Small RNAs-the secret agents in the plant-pathogen interactions. Current Opinion in Plant Biology 26: 87-94.
Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342: 118-123.
Wiggers RJJ, Starr JLL, Price HJJ. 1990. DNA content and variation in chromosome number in plant cells affected by Meloidogyne incognita and M. arenaria. Phytopathology 80: 1391-1395.
Xu W, Meng Y, Wise RP. 2014. Mla- and Rom1-mediated control of microRNA398 and chloroplast copper/zinc superoxide dismutase regulates cell death in response to the barley powdery mildew fungus. New Phytologist 201: 1396-1412.
Yamaguchi YL, Suzuki R, Cabrera J, Nakagami S, Sagara T, Ejima C, Sano R, Aoki Y, Olmo R, Kurata T et al. 2017. Root-knot and cyst nematodes activate procambium-associated genes in Arabidopsis roots. Frontiers in Plant Science 8: 1-13.
Yamasaki H, Abdel-Ghany SE, Cohu CM, Kobayashi Y, Shikanai T, Pilon M. 2007. Regulation of copper homeostasis by micro-RNA in Arabidopsis. Journal of Biological Chemistry 282: 16369-16378.
Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T. 2009. SQUAMOSA promoter binding protein-like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21: 347-361.
Zhang H, Li L. 2013. SQUAMOSA promoter binding protein-like7 regulated microRNA408 is required for vegetative development in Arabidopsis. The Plant Journal 74: 98-109.
Zhang H, Zhao X, Li J, Cai H, Deng XW, Li L. 2014. Microrna408 is critical for the HY5-SPl7 gene network that mediates the coordinated response to light and copper. Plant Cell 26: 4933-4953.
Zhang J-P, Yu Y, Feng Y-Z, Zhou Y-F, Zhang F, Yang Y-W, Lei M-Q, Zhang Y-C, Chen Y-Q. 2017. MiR408 regulates grain yield and photosynthesis via a phytocyanin protein. Plant Physiology 175: 1175-1185.
Zhao J, Mejias J, Quentin M, Chen Y, de Almeida-Engler J, Mao Z, Sun Q, Liu Q, Xie B, Abad P et al. 2020. The root-knot nematode effector MiPDI1 targets a stress-associated protein (SAP) to establish disease in Solanaceae and Arabidopsis. New Phytologist 228: 1417-1430.