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Potato NAC43 and MYB8 Mediated Transcriptional Regulation of Secondary Cell Wall Biosynthesis to Contain Phytophthora infestans Infection

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Abstract

Resistance to late blight is highly complex and quantitative in nature but has proven difficult to harness due to poor understanding of its molecular and biochemical mechanisms. Secondary cell wall (SCW) biosynthesis is a critical process in late blight resistance, regulated by an array of transcription factors (TF). In the present study, metabolo-transcriptomics approaches were used to functionally characterize that the upregulated StNAC43 and StMYB8 in potato genotypes were linked to SCW biosynthetic phenylpropanoid metabolites produced in high fold change following Phytophthora infestans infection. The promoter analysis of StNAC43 revealed the presence of ethylene responsive element (ERE), which is the proposed binding site for ethylene responsive factor, ERF3. Sequencing of the ERF3 revealed a frameshift mutation in the susceptible potato genotype. Simultaneous induction of both the ERF3 and StNAC43, following pathogen invasion, enables functioning of the latter to interact with the ERE present in the resistant StNAC43 promoter region. Further, the StNAC43 binds to the secondary NAC binding element in StMYB8 promoter and activates StMYB8 TF. A luciferase transient expression assay elucidated a direct regulatory role of the StMYB8 on SCW biosynthetic genes, by binding to promoters of downstream genes: HCT, PHT, CHS, and flavanone 3-hydroxylase (F3H). Silencing of StNAC43 and StMYB8 affected the late blight resistance by significantly increasing pathogen biomass and decreasing the amounts of hydroxycinnamic acid amides (HCAAs) and flavonoid glycosides. The StNAC43 and StMYB8 TFs are positive activators of SCW biosynthetic genes, which deposit resistance-related metabolites to reinforce SCW and improve resistance against late blight.

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Abbreviations

SCW:

Secondary cell wall

TF:

Transcription factor

ERF:

Ethylene responsive factor

ERE:

Ethylene responsive elements

RR:

Resistance-related

RRI:

Resistance-related induced

RRC:

Resistance-related constitutive

HCAAs:

Hydroxycinnamic acid amides

HCT:

Hydroxycinnamoyl transferase

PHT:

Putrescine hydroxycinnamoyl transferase

CHS:

Chalcone synthase

F3H:

Flavanone 3-hydroxylase

References

  • Alemanno L, Ramos T, Gargadenec A, Andary C, Ferriere N (2003) Localization and identification of phenolic compounds in Theobroma cacao L. somatic embryogenesis. Ann Bot 92:613–623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buscaill P, Rivas S (2014) Transcriptional control of plant defence responses. Curr Opin Plant Biol 20:35–46

    Article  CAS  PubMed  Google Scholar 

  • Chai M, Bellizzi M, Wan C, Cui Z, Li Y, Wang G-L (2015) The NAC transcription factor OsSWN1 regulates secondary cell wall development in Oryza sativa. J Plant Biol 58:44–51

    Article  CAS  Google Scholar 

  • Cheng H-Q, Han L-B, Yang C-L, Wu X-M, Zhong N-Q, Wu J-H, Wang F-X, Wang H-Y, Xia G-X (2016) The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. J Exp Bot 67:1935–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 46:521–529

    Article  CAS  PubMed  Google Scholar 

  • DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, Philippakis AA, Del Angel G, Rivas MA, Hanna M (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43:491–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunnaiah R, Kushalappa AC, Duggavathi R, Fox S, Somers DJ (2012) Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PloS One 7:e40695

  • Haverkort A, Struik P, Visser R, Jacobsen E (2009) Applied biotechnology to combat late blight in potato caused by Phytophthora infestans. Potato Res 52:249–264

    Article  Google Scholar 

  • Huang P-Y, Catinot J, Zimmerli L (2015) Ethylene response factors in Arabidopsis immunity. J Exp Bot 67:1231–1241

    Article  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kage U, Yogendra KN, Kushalappa AC (2017) TaWRKY70 transcription factor in wheat QTL-2DL regulates downstream metabolite biosynthetic genes to resist Fusarium graminearum infection spread within spike. Sci Rep 7

  • Kaur H, Heinzel N, Schöttner M, Baldwin IT, Gális I (2010) R2R3-NaMYB8 regulates the accumulation of phenylpropanoid-polyamine conjugates, which are essential for local and systemic defense against insect herbivores in Nicotiana attenuata. Plant Physiol 152:1731–1747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee B-K, Rupak T, Jeong H, Lee Y, Hong BS (2014) Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J Exp Bot 65:4023–4036

    Article  PubMed  PubMed Central  Google Scholar 

  • Kou Y, Wang S (2010) Broad-spectrum and durability: understanding of quantitative disease resistance. Curr Opin Plant Biol 13:181–185

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Campbell L, Turner S (2015) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531

    Article  PubMed  Google Scholar 

  • Kumar A, Yogendra KN, Karre S, Kushalappa AC, Dion Y, Choo TM (2016) WAX INDUCER1 (HvWIN1) transcription factor regulates free fatty acid biosynthetic genes to reinforce cuticle to resist Fusarium head blight in barley spikelets. J Exp Bot 67:4127–4139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kushalappa AC, Gunnaiah R (2013) Metabolo-proteomics to discover plant biotic stress resistance genes. Trends Plant Sci 18:522–531

    Article  CAS  PubMed  Google Scholar 

  • Kushalappa AC, Yogendra KN, Karre S (2016a) Plant innate immune response: qualitative and quantitative resistance. Crit Rev Plant Sci 35:38–55

    Article  CAS  Google Scholar 

  • Kushalappa AC, Yogendra KN, Sarkar K, Kage U, Karre S (2016b) Gene discovery and genome editing to develop cisgenic crops with improved resistance against pathogen infection. Can J Plant Pathol. doi:10.1080/07060661.2016.1199597

  • Le Hénanff G, Profizi C, Courteaux B, Rabenoelina F, Gérard C, Clément C, Baillieul F, Cordelier S, Dhondt-Cordelier S (2013) Grapevine NAC1 transcription factor as a convergent node in developmental processes, abiotic stresses, and necrotrophic/biotrophic pathogen tolerance. J Exp Bot 64:4877–4893

    Article  PubMed  Google Scholar 

  • Legay S, Sivadon P, Blervacq AS, Pavy N, Baghdady A, Tremblay L, Levasseur C, Ladouce N, Lapierre C, Séguin A (2010) EgMYB1, an R2R3 MYB transcription factor from eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar. New Phytol 188:774–786

    Article  CAS  PubMed  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Schiff M, Dinesh-Kumar S (2002) Virus-induced gene silencing in tomato. Plant J 31:777–786

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • López-Gresa MP, Torres C, Campos L, Lisón P, Rodrigo I, Bellés JM, Conejero V (2011) Identification of defence metabolites in tomato plants infected by the bacterial pathogen Pseudomonas syringae. Environ Exper Bot 74:216–228

    Article  Google Scholar 

  • McCarthy RL, Zhong R, Ye Z-H (2009) MYB83 is a direct target of SND1 and acts redundantly with MYB46 in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell Physiol 50:1950–1964

    Article  CAS  PubMed  Google Scholar 

  • McCarthy RL, Zhong R, Fowler S, Lyskowski D, Piyasena H, Carleton K, Spicer C, Ye Z-H (2010) The poplar MYB transcription factors, PtrMYB3 and PtrMYB20, are involved in the regulation of secondary wall biosynthesis. Plant Cell Physiol 51:1084–1090

    Article  CAS  PubMed  Google Scholar 

  • McCarthy RL, Zhong R, Ye Z-H (2011) Secondary wall NAC binding element (SNBE), a key cis-acting element required for target gene activation by secondary wall NAC master switches. Plant Signal Behav 6:1282–1285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front Plant Sci 6.

  • Nicot N, Hausman J-F, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56:2907–2914

    Article  CAS  PubMed  Google Scholar 

  • Nuruzzaman M, Sharoni AM, Kikuchi S (2015) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4:248

    Google Scholar 

  • Onkokesung N, Gaquerel E, Kotkar H, Kaur H, Baldwin IT, Galis I (2012) MYB8 controls inducible phenolamide levels by activating three novel hydroxycinnamoyl-coenzyme A: polyamine transferases in Nicotiana attenuata. Plant Physiol 158:389–407

    Article  CAS  PubMed  Google Scholar 

  • Pluskal T, Castillo S, Villar-Briones A, Orešič M (2010) MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics 11:395

    Article  PubMed  PubMed Central  Google Scholar 

  • Pushpa D, Yogendra KN, Gunnaiah R, Kushalappa AC, Murphy A (2014) Identification of late blight resistance-related metabolites and genes in potato through nontargeted metabolomics. Plant Mol Biol Rep 32:584–595

    Article  CAS  Google Scholar 

  • Rong W, Qi L, Wang A, Ye X, Du L, Liang H, Xin Z, Zhang Z (2014) The ERF transcription factor TaERF3 promotes tolerance to salt and drought stresses in wheat. Plant Biotechnol J 12:468–479

    Article  CAS  PubMed  Google Scholar 

  • Sun L, Zhang H, Li D, Huang L, Hong Y, Ding XS, Nelson RS, Zhou X, Song F (2013) Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magnaporthe grisea. Plant Mol Biol 81:41–56

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Gong SY, Nie XY, Li Y, Li W, Huang GQ, Li XB (2015) A R2R3-MYB transcription factor that is specifically expressed in cotton (Gossypium hirsutum) fibers affects secondary cell wall biosynthesis and deposition in transgenic Arabidopsis. Physiol Plant 154:420–432

    Article  CAS  PubMed  Google Scholar 

  • Tsuda K, Somssich IE (2015) Transcriptional networks in plant immunity. New Phytol 206:932–947

    Article  CAS  PubMed  Google Scholar 

  • Velivelli SLS, Lojan P, Cranenbrouck S, de Boulois HD, Suarez JP, Declerck S, Franco J, Prestwich BD (2015) The induction of ethylene response factor 3 (ERF3) in potato as a result of co-inoculation with Pseudomonas sp. R41805 and Rhizophagus irregularis MUCL 41833—a possible role in plant defense. Plant Signal Behav 10:e988076.

  • Wang H-Z, Dixon RA (2012) On–off switches for secondary cell wall biosynthesis. Mol Plant 5:297–303

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Li E, Porth I, Chen J-G, Mansfield SD, Douglas CJ (2014) Regulation of secondary cell wall biosynthesis by poplar R2R3 MYB transcription factor PtrMYB152 in Arabidopsis. Sci Rep 4

  • Wang F, Lin R, Feng J, Chen W, Qiu D, Xu S (2015) TaNAC1 acts as a negative regulator of stripe rust resistance in wheat, enhances susceptibility to Pseudomonas syringae, and promotes lateral root development in transgenic Arabidopsis thaliana. Front Plant Sci 6

  • Watanabe K (2015) Potato genetics, genomics, and applications. Breeding Sci 65:53

    Article  Google Scholar 

  • Weigel D, Glazebrook J (2006) Transformation of agrobacterium using the freeze-thaw method. CSH protocols 7

  • Wen W, Li D, Li X, Gao Y, Li W, Li H, Liu J, Liu H, Chen W, Luo J (2014) Metabolome-based genome-wide association study of maize kernel leads to novel biochemical insights. Nat Commun 5

  • Yogendra KN, Kushalappa AC (2016) Integrated transcriptomics and metabolomics reveal induction of a hierarchy of resistance genes in potato against late blight. Funct Plant Biol 43:766–782

    Article  CAS  Google Scholar 

  • Yogendra KN, Pushpa D, Mosa KA, Kushalappa AC, Murphy A, Mosquera T (2014) Quantitative resistance in potato leaves to late blight associated with induced hydroxycinnamic acid amides. Funct Integr Genomic 14:285–298

    Article  CAS  Google Scholar 

  • Yogendra KN, Kumar A, Sarkar K, Li Y, Pushpa D, Mosa KA, Duggavathi R, Kushalappa AC (2015a) Transcription factor StWRKY1 regulates phenylpropanoid metabolites conferring late blight resistance in potato. J Exp Bot 66:7377–7389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yogendra KN, Kushalappa AC, Sarmiento F, Rodriguez E, Mosquera T (2015b) Metabolomics deciphers quantitative resistance mechanisms in diploid potato clones against late blight. Funct Plant Biol 42:284–298

    CAS  Google Scholar 

  • Yogendra KN, Dhokane D, Kushalappa AC, Sarmiento F, Rodriguez E, Mosquera T (2017) StWRKY8 transcription factor regulates benzylisoquinoline alkaloid pathway in potato conferring resistance to late blight. Plant Sci 256:208–216

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Yao W, Dong N, Liang H, Liu H, Huang R (2007) A novel ERF transcription activator in wheat and its induction kinetics after pathogen and hormone treatments. J Exp Bot 58:2993–3003

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Ye Z-H (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53:368–380

    Article  CAS  PubMed  Google Scholar 

  • Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H (2008) A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell 18:3158–3170

    Article  Google Scholar 

  • Zhong R, Yuan Y, Spiekerman JJ, Guley JT, Egbosiuba JC, Ye Z-H (2015) Functional characterization of NAC and MYB transcription factors involved in regulation of biomass production in switchgrass (Panicum virgatum). PloS One 10:e0134611

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Acknowledgements

This work was carried out with the aid of a grant from the Natural Sciences and Engineering Council of Canada (NSERC) and the International Development Research Center (IDRC), Canada, with the financial support of the Department of Foreign Affairs, Trade and Development Canada (DFATD).

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K.N.Y. and A.C.K. planned and designed the research. K.N.Y. and K.S. conducted greenhouse work, performed the experiments, and analyzed the data. K.N.Y. and A.C.K. wrote the manuscript. All authors have read and approved the manuscript.

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Correspondence to Ajjamada C. Kushalappa.

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Yogendra, K.N., Sarkar, K., Kage, U. et al. Potato NAC43 and MYB8 Mediated Transcriptional Regulation of Secondary Cell Wall Biosynthesis to Contain Phytophthora infestans Infection. Plant Mol Biol Rep 35, 519–533 (2017). https://doi.org/10.1007/s11105-017-1043-1

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