Cross-kingdom microRNA transfer for the control of the anthracnose disease in cassava

Tropical Plant Pathology - Tập 47 Số 3 - Trang 362-377
Nattaya Pinweha1,2, Supatcharee Netrphan3, Punchapat Sojikul2, Unchera Viboonjun4, Pakatorn Sae-Lim2, Jarunya Narangajavana1,2
1Center of Excellence On Agricultural Biotechnology: (AG-BIO/MHESI), Bangkok, Thailand
2Department of Biotechnology, Faculty of Science, Mahidol University, Bangkok, Thailand
3National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency, Pathum Thani, Thailand
4Department of Plant Science, Faculty of Science, Mahidol University, Bangkok, Thailand

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Alvarez ME, Pennell RI, Meijer P, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

Bredeson JV, Lyons JB, Prochnik SE, Wu GA, Ha CM, Edsinger-Gonzales E, Grimwood J, Schmutz J, Rabbi IY, Egesi C, Nauluvula P, Lebot V, Ndunguru J, Mkamilo G, Bart RS, Setter TL, Gleadow RM, Kulakow P, Ferguson ME, Rounsley S, Rokhsar DS (2016) Sequencing wild and cultivated cassava and related species reveals extensive interspecific hybridization and genetic diversity. Nature Biotechnology 34:562–570

Cai Q, Qiao L, Wang M, He B, Lin F, Palmquist J, Huang S, Jin H (2018) Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–1129

Cano J, Guarro J, Gend J (2004) Molecular and morphological identification of Colletotrichum species of clinical interest. Journal of Clinical Microbiology 42:2450–2454

Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proceedings of the National Academy of Sciences of the Unites States of America 102:3459–3464

Chen X, Zhang Z, Liu D, Zhang K, Li A, Mao L (2010) SQUAMOSA promoter-binding protein-like transcription factors; star players for plant growth and development. Journal of Integrative Plant Biology 52:946–951

Cheng H, Gao J, An Z, Huang H (2010) A rapid method for isolation of low-molecular-weight RNA from Arabidopsis using low salt concentration buffer. Integrative Journal of Plant Biology 1:e14

Choi J, Kim K, Jeon J, Wu J, Song H, Asiegbu FO, Lee Y (2014) funRNA: a fungi-centered genomics platform for genes encoding key components of RNAi. BMC Genomics 15:514

Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research 39:W155–W159

Daudi A, O’Brien JA (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis leaves. Bio-protocol 2:e263

Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15

Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somervilles SC, Voigt CA (2013) Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiology 161:1433–1444

Feng H, Duan X, Zhang Q, Li X, Wang B, Huang L, Wang X, Kang Z (2014) The target gene of tae-miR164, a novel NAC transcription factor from the NAM family, negatively regulates resistance of wheat to stripe rust. Molecular Plant Pathology 15:284–296

Fokunang CN, Akem CN, Ikotun T, Dixon AGO, Tembe EA (2000) Role of the insect vector, Pseudotheraptus devastans, in cassava anthracnose disease development. European Journal of Plant Pathology 106:319–237

Fokunang CN, Dixon AGO, Ikotun T, Tembe EA, Akem CN, Asiedu R (2001) Anthracnose: an economic disease of cassava in Africa. Pakistan Journal of Biological Science 4:920–925

Gacek-Matthews A, Berger H, Sasaki T, Wittstein K, Gruber C, Lewis ZA, Strauss J (2016) KdmB, a jumonji histone H3 demethylase, regulates genome-wide H3K4 trimethylation and is required for normal induction of secondary metabolism in Aspergillus nidulans. PLoS Genetics 12:e1006222

Gundersen GG, Worman HJ (2013) Nuclear positioning. Cell 152:1376–1389

Gupta OP, Sharma P, Gupta RK, Sharma I (2014) Current status on role of miRNAs during plant-fungus interaction. Physiological and Molecular Plant Pathology 85:1–7

Hagen I, Yanagida M (1995) The product of the spindle formation gene sad1+ associates with the fission yeast spindle pole body and is essential for viability. Journal of Cell Biology 129:1033–1047

Hahn SK, Ikotun T, Theberge RL, Swennen R (1989) Major economic diseases of cassava, plantains and cooking starchy bananas in Africa. Tropical Agricultural Research Series 22:106–112

Hou J, Feng H, Chang H, Liu Y, Li G, Yang S, Sun C, Zhang M, Yuan Y, Sun J, Zhu-Salzman K, Zhang H, Qin Q (2020) The H3K4 demethylase Jar1 orchestrates ROS production and expression of pathogenesis-related genes to facilitate Botrytis cinerea virulence. New Phytologist 225:930–947

Howe KL, Contreras-Moreira B, De Silva N, Maslen G, Akanni W, Allen J, Alvarez-Jarreta J, Barba M, Bolser DM, Cambell L, Carbajo M, Chakiachvili M, Christensen M, Cummins C, Cuzick A, Davis P, Fexova S, Gall A, George N, Gil L, Gupta P, Hammond-Kosack KE, Haskell E, Hunt SE, Jaiswal P, Janacek SH, Kersey PJ, Langridge N, Maheswari U, Maurel T, McDowall MD, Moore B, Muffato M, Naamati G, Naithani S, Olson A, Papatheodorou I, Patricio M, Paulini M, Pedro H, Perry E, Preece J, Rosello M, Russell M, Sitnik V, Staines DM, Stein J, Tello-Ruiz MK, Trevanion ST, Urban M, Wei S, Ware D, Williams G, Yates AD, Flicek P (2020) Ensembl Genomes 2020-enabling non-vertebrate genomic research. Nucleic Acids Research 48:D689–D695

Hu G, Lei Y, Liu J, Hao M, Zhang Z, Tang Y, Chen A, Wu J (2020) The ghr-miR164 and GhNAC100 modulate cotton plant resistance against Verticillium dahlia. Plant Science 293:110438

Iwakawa H, Tomari Y (2015) The functions of microRNAs: mRNA decay and translational repression. Trends in Cell Biology 25:651–665

Kim JW, Shim SH (2019) The fungus Colletotrichum as a source for bioactive secondary metabolites. Archives of Pharmacal Research 42:735–753

Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus flower meristem identity gene SQUAMOSA. Molecular and General Genetics 250:7–16

Klemm E, Ninnemann H (1978) Correlation between absorbance changes and a physiological response induced by blue light in Neurospora crassa. Photochemistry and Photobiology 28:227–230

Kunkeaw S, Worapun J, Smith DR, Triwitayakorn K (2010) An in vitro detached leaf assay for pre-screening resistance to anthracnose disease in cassava (Manihot esculenta Crantz). Australasian Plant Pathology 39:547–550

Lee SC, Hwang BK (2005) Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221:790–800

Lertpanyasampatha M, Viboonjun U, Kongsawadworakul P, Chrestin H, Narangajavana J (2014) Differential expression of microRNAs and their targets reveals a possible dual role in physiological bark disorder in rubber tree. Journal of Plant Physiology 171:1117–1126

Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30:325–327

Li B, Meng X, Shan L, He P (2016) Transcriptional regulation of pattern-triggered immunity in plants. Cell Host & Microbe 19:641–650

Liu Y, He Q, Cheng P (2003) Photoreception in Neurospora: a tale of two White Collar proteins. Cellular and Molecular Life Sciences 60:2131–2138

Liu M, Shi Z, Zhang X, Wang M, Zhang L, Zheng K, Liu J, Hu X, Di C, Qian Q, He Z, Yng D (2019) Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nature Plants 5:389–400

Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. Molecular Plant-Microbe Interactions 24:183–193

Mahto BK, Singh A, Pareek M, Rajam MV, Dhar-Ray S, Reddy PM (2020) Host-induced silencing of the Colletotrichum gloeosporioides conidial morphology 1 gene (CgCOM1) confers resistance against Anthracnose disease in chilli and tomato. Plant Molecular Biology 104:381–395

Malone CJ, Fixsen WD, Moritz R, Han M (1999) UNC-84 localizes to the nuclear envelope and is required for nuclear migration and anchoring during C. elegans development. Development 126:3171–3181

Marzluf GA (1997) Genetic regulation of nitrogen metabolism in the fungi. Microbiology and Molecular Biology Reviews 61:17–32

McCallum EJ, Anjanappa RB, Gruissem W (2017) Tacking agriculturally relevant diseases in the staple crop cassava (Manihot esculenta). Current Opinion in Plant Biology 38:50–58

Moraga J, Gomes W, Pinedo C, Cantoral JM, Hanson JR, Carbu M, Garrido C, Durán-Patrón R, Collada IG (2019) The current status on secondary metabolites produced by plant pathogenic Colletotrichum species. Phytochemistry Reviews 18:215–239

Nakashima J, Laosinchai W, Cui X, Brown RM (2003) New insight into the mechanism of cellulose and callose biosynthesis; protease may regulate callose biosynthesis upon wounding. Cellulose 10:369–389

Nedukha OM (2015) Callose: localization, functions, and synthesis in plant cells. Cytology and Genetics 49:49–57

O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779

Owolade OF, Dixon AGO, Adeoti AA, Osunlaja SO (2005) Sources of resistance to cassava anthracnose disease. African Journal of Biotechnology 4:570–572

Panwar SL, Moye-Rowley WS (2006) Long chain base tolerance in Saccharomyces cerevisiae is induced by retrograde signals from the mitochondria. Journal of Biological Chemistry 281:6376–6384

Perfect SE, Hughes HB, O’Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal-plant interactions. Fungal Genetics and Biology 27:186–198

Perino EHB, Glienke C, Silva AO, Deising HB (2020) Molecular characterization of the purine degradation pathways genes ALA1 and URE1 of the maize anthracnose fungus Colletotrichum graminicola identified urease as a novel target for plant disease control. Phytopathology 110:1530–1540

Pinweha N, Asvarak T, Viboonjun U, Narangajavana J (2015) Involvement of miR160/miR393 and their targets in cassava responses to anthracnose disease. Journal of Plant Physiology 174:26–35

Piršelová B, Matušíková I (2013) Callose: the plant cell wall polysaccharide with multiple biological functions. Acta Physiologiae Plantarum 35:635–644

Riddell RW (1950) Permanent stained mycological preparations obtained by slide culture. Mycologia 42:265–270

Saelim L, Phansiri S, Suksangpanomrung M, Netrphan S, Narangajavana J (2009) Evaluation of a morphological marker selection and excision system to generate marker-free transgenic cassava plants. Plant Cell Reports 28:445–455

Scalschi L, Llorens E, Camañes G, Pastor V, Fernández-Crespo E, Flors V, García-Agustín P, Vicedo B (2015) Quantification of callose deposition in plant leaves. Bio-protocol 5:e1610

Schjoerring JK, Husted S, Mack G, Mattsson M (2002) The regulation of ammonium translation in plants. Journal of Experimental Botany 53:883–890

Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Developmental Cell 8:517–527

Solomon PS, Oliver RP (2001) The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 213:241–249

Stief A, Altmann S, Hoffmann K, Pant BD, Scheible W-R, Baurle I (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26:1792–1807

Tetyuk O, Benning UF, Hoffmann-Benning S (2013) Collection and analysis of Arabidopsis phloem exudates using the EDTA-facilitated method. Journal of Visualized Experiments 80:e51111

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Research 40:e115

Valle EM, Boggio SB, Heldt HW (1998) Free amino acid composition of phloem sap and growing fruit of Lycopersicon esculentum. Plant and Cell Physiology 39:458–461

Varkonyi-Gasic E, Wu R, Wood M, Walton EF, Hellens RP (2007) Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs. Plant Methods 3:12

Walker SE, Lorsch J (2013) RNA purification - precipitation methods. Methods in Enzymology 530:337–343

Wang M, Weiberg A, Lin F, Thomma BPHJ, Huang H, Jin H (2016) Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nature Plants 2:16151

Wang B, Sun Y, Song N, Zhao M, Liu R, Feng H, Wang X, Kang Z (2017) Puccinia striiformis f. sp. tritici microRNA-like RNA1 (Pst-milR1), and important pathogenicity factor of Pst, impairs wheat resistance to Pst by suppressing the wheat pathogenesis-related 2 gene. New Phytologist 215:338–350

Wang Z, Xia Y, Lin S et al (2018) Osa-miR164a targets OsNAC60 and negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Plant Journal 95:584–597

Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

Wu L, Chen H, Curtis C, Fu ZQ (2014) Go in for the kill: how plants deploy effector-triggered immunity to combat pathogens. Virulence 5:710–721

Yin H, Hong G, Li L, Zhang X, Kong Y, Sun Z, Li J, Chen J, He Y (2019) miR156/SPL9 regulates reactive oxygen species accumulation and immune response in Arabidopsis thaliana. Phytopathology 109:612–642

Yu N, Niu Q, Ng K, Chua N (2015) The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant Journal 83:673–685

Zhang T, Zhao Y, Zhao J, Wang S, Jin Y, Chen Z, Fang Y, Hua C, Ding S, Guo H (2016) Cotton plants export microRNAs to inhibit virulence gene expression in a fungal pathogen. Nature Plants 2:16153

Zhang Q, Li Y, Zhang Y, Wu C, Wang S, Hao L, Wang S, Li T (2017) Md-miR156ab and Md-miR395 target WRKY transcription factors to influence apple resistance to leaf spot disease. Frontiers in Plant Science 8:526

Zhang L, Li Y, Zheng Y, Wang H, Yang X, Chen J, Zhou S, Wang L, Li X, Ma X, Zhao J, Pu M, Feng H, Fan J, Zhang J, Huang Y, Wang W (2020) Expression a target mimic of miR156fhl-3p enhances rice blast disease resistance without yield penalty by improving SPL14 expression. Frontiers in Genetics 11:327

Zhou G, Zhou Y, Chen X (2017) New insight into inter-kingdom communication: horizontal transfer of mobile small RNAs. Frontiers in Microbiology 8:768

Zipfel C, Felix G (2005) Plants and animals: a different taste for microbes? Current Opinion in Plant Biology 8:353–360