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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

NAC transcription factor involves in regulating bacterial wilt resistance in potato

Yannan Chang A , Ruimin Yu A , Jinlin Feng B , Huize Chen B , Hemu Eri C and Gang Gao orcid.org/0000-0002-0705-1316 A D
+ Author Affiliations
- Author Affiliations

A Genetic Engineering Laboratory, College of Life Science, Shanxi Normal University, Linfen 041000, China.

B Cell Biology Laboratory, College of Life Science, Shanxi Normal University, Linfen 041000, China.

C Function Food Laboratory, College of Food Science, Shanxi Normal University, Linfen 041000, China.

D Corresponding author. Email: ggsxnu@126.com

Functional Plant Biology 47(10) 925-936 https://doi.org/10.1071/FP19331
Submitted: 17 November 2019  Accepted: 27 April 2020   Published: 27 May 2020

Abstract

Bacterial wilt (BW) is a serious disease that affects potato (Solanum tuberosum L.) production. Although resistance to this disease has been reported, the underlying mechanism is unknown. In this study, we identified a NAC family transcription factor (StNACb4) from potato and characterised its structure, function, expression, its localisation at the tissue and its role in BW resistance. To this end, the transgenic Nicotiana benthamiana Domin lines were generated in which the expression of NACb4 was constitutively upregulated or suppressed using RNAi. Different tobacco mutants were stained after inoculating with Ralstonia solanacearum to observe the cell death and callose deposition. The results indicated that StNACb4 could be upregulated under the induction of R. solanacearum, and salicylic acid, abscisic acid and methyl jasmonate could also induce the expression of StNACb4. Tissue localisation analysis indicated that its expression was tissue specific, and it was mainly in the phloem of the vascular system of stems and leaves. NbNACb4 gene silencing can enhance the sensitivity of tobacco to R. solanacearum; on the contrary, StNACb4 gene overexpression can enhance the tolerance of tobacco to R. solanacearum. Meanwhile, StNACb4 gene overexpression can induce cell death and callose deposition in tobacco. The upregulated expression of StNACb4 can also activate the StPR10 gene expression. Our results provide important new insights into the regulatory mechanisms of bacterial wilt resistance in potato.

Additional keywords: callose deposition, cell death, Ralstonia solanacearum, StNACb4, transgenic tobacco.


References

Abdurahman A, Parker ML, Kreuze J, Elphinstone JG, Struik PC, Kigundu A, Arengo E, Sharma K (2019) Molecular epidemiology of Ralstonia solanacearum species complex strains causing bacterial wilt of potato in Uganda. Phytopathology 109, 1922–1931.
Molecular epidemiology of Ralstonia solanacearum species complex strains causing bacterial wilt of potato in Uganda.Crossref | GoogleScholarGoogle Scholar | 31272278PubMed |

Ali S, Ganai BA, Kamili AN, Bhat AA, Mir ZA, Bhat JA, Tyagi A, Islam ST, Mushtaq M, Yadav P, Rawat S, Grover A (2018) Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiological Research 212–213, 29–37.
Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance.Crossref | GoogleScholarGoogle Scholar | 29853166PubMed |

Balazadeh S, Siddiqui H, Ad A, Lp MR, Caldana C, Mehrnia M (2010) A gene regulatory network controlled by the NAC transcription factor ANAC092/ATNAC2/ORE1 during salt-promoted senescence. The Plant Journal 62, 250–264.
A gene regulatory network controlled by the NAC transcription factor ANAC092/ATNAC2/ORE1 during salt-promoted senescence.Crossref | GoogleScholarGoogle Scholar | 20113437PubMed |

Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324, 742–744.
Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens.Crossref | GoogleScholarGoogle Scholar | 19423812PubMed |

Broderick K, Pittock C, Arioli T, Creaser EH, Weinman JJ, Rolfe BG (1997) Pathogenesis-related proteins in Trifolium subterraneum: a general survey and subsequent characterisation of a protein inducible by ethephon and redlegged earth mite attack. Functional Plant Biology 24, 819–829.
Pathogenesis-related proteins in Trifolium subterraneum: a general survey and subsequent characterisation of a protein inducible by ethephon and redlegged earth mite attack.Crossref | GoogleScholarGoogle Scholar |

Chen Q, Niu F, Yan J, Chen B, Wu F, Guo X (2017) Oilseed rape NAC56 transcription factor modulates reactive oxygen species accumulation and hypersensitive response-like cell death. Physiologia Plantarum 160, 209–221.
Oilseed rape NAC56 transcription factor modulates reactive oxygen species accumulation and hypersensitive response-like cell death.Crossref | GoogleScholarGoogle Scholar | 28097691PubMed |

Cheng Y, Zhang H, Yao J, Wang X, Xu J, Han Q, Kang Z (2012) Characterization of non-host resistance in broad bean to the wheat stripe rust pathogen. BMC Plant Biology 12, 96–107.
Characterization of non-host resistance in broad bean to the wheat stripe rust pathogen.Crossref | GoogleScholarGoogle Scholar | 22716957PubMed |

Chowdury R, Lasky D, Karki H, Zhang Z, Goyer A, Halterman D, Rakotondrafara AM (2019) HCPro suppression of callose deposition contributes to strain specific resistance against potato virus Y. Phytopathology 110, 164–173.
HCPro suppression of callose deposition contributes to strain specific resistance against potato virus Y.Crossref | GoogleScholarGoogle Scholar |

Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323, 95–101.
Glucosinolate metabolites required for an Arabidopsis innate immune response.Crossref | GoogleScholarGoogle Scholar | 19095898PubMed |

Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death and Differentiation 18, 1247–1256.
Programmed cell death in the plant immune system.Crossref | GoogleScholarGoogle Scholar | 21475301PubMed |

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 Molecular Biology 46, 521–529.
Differential induction of two potato genes, StPRX2 and StNAC, in response to infection by Phytophthora infestans and to wounding.Crossref | GoogleScholarGoogle Scholar | 11516145PubMed |

Crowley LC, Marfell BJ, Christensen ME, Waterhouse NJ (2016) Measuring cell death by trypan blue uptake and light microscopy. Cold Spring Harbor Protocols 2016, 643–646.
Measuring cell death by trypan blue uptake and light microscopy.Crossref | GoogleScholarGoogle Scholar |

Dobnik D, Lazar A, Stare T, Gruden K, Vleeshouwers VGAA, Žel J (2016) Solanum venturii, a suitable model system for virus-induced gene silencing studies in potato reveals StMKK6 as an important player in plant immunity. Plant Methods 12, 29
Solanum venturii, a suitable model system for virus-induced gene silencing studies in potato reveals StMKK6 as an important player in plant immunity.Crossref | GoogleScholarGoogle Scholar | 27213007PubMed |

Feng H, Duan X, Zhang Q, Li X, Wang B, Huang L (2014) The target gene of tae-miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust. Molecular Plant Pathology 15, 284–296.
The target gene of tae-miR164, a novel NAC transcription factor from the NAM subfamily, negatively regulates resistance of wheat to stripe rust.Crossref | GoogleScholarGoogle Scholar | 24128392PubMed |

Hall TA (1999) BioEdit, a user-friendly biological sequence alignment and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. The Plant journal: for cell and molecular biology 68, 302–313.
Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants.Crossref | GoogleScholarGoogle Scholar |

He LY (1983) Characteristics of strains of Ralstonia solanacearum from China. Plant Disease 67, 1357–1361.
Characteristics of strains of Ralstonia solanacearum from China.Crossref | GoogleScholarGoogle Scholar |

He Q, McLellan H, Boevink PC, Sadanandom A, Xie C, Birch PRJ, Tian Z (2015) U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. Journal of Experimental Botany 66, 3189–3199.
U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar | 25873665PubMed |

He X, Zhu L, Xu L, Guo W, Zhang X (2016) GhATAF1, a NAC transcription factor, confers abiotic and biotic stress responses by regulating phytohormonal signaling networks. Plant Cell Reports 35, 2167–2179.
GhATAF1, a NAC transcription factor, confers abiotic and biotic stress responses by regulating phytohormonal signaling networks.Crossref | GoogleScholarGoogle Scholar | 27432176PubMed |

Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Molecular Biology 53, 383–397.
Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 14750526PubMed |

Huang QJ, Wang Y, Li B, Chang JL, Chen MJ, Li KX, Yang GX, He GY (2015) TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis. BMC Plant Biology 15, 268
TaNAC29, a NAC transcription factor from wheat, enhances salt and drought tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Ismail Y, Hijri M (2012) Arbuscular mycorrhisation with Glomus irregulare induces expression of potato PR homologues genes in response to infection by Fusarium sambucinum. Functional Plant Biology 39, 236–245.
Arbuscular mycorrhisation with Glomus irregulare induces expression of potato PR homologues genes in response to infection by Fusarium sambucinum.Crossref | GoogleScholarGoogle Scholar |

Jensen MK, Hagedorn PH, De Torres‐Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF (2008) Transcriptional regulation by an NAC (NAM-ATAF1, 2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f.sp. hordei in Arabidopsis. The Plant Journal 56, 867–880.
Transcriptional regulation by an NAC (NAM-ATAF1, 2-CUC2) transcription factor attenuates ABA signalling for efficient basal defence towards Blumeria graminis f.sp. hordei in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 18694460PubMed |

Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
The plant immune system.Crossref | GoogleScholarGoogle Scholar |

Kaneda T, Taga Y, Takai R, Iwano M, Matsui H, Takayama S, Isogai A, Chen FS (2009) The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. EMBO Journal 28, 926–936.
The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death.Crossref | GoogleScholarGoogle Scholar | 19229294PubMed |

Kim SG, Kim SY, Park CM (2007) A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Planta 226, 647–654.
A membrane-associated NAC transcription factor regulates salt-responsive flowering via FLOWERING LOCUS T in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17410378PubMed |

Kim SG, Lee AK, Yoon HK, Park CM (2008) A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination. The Plant journal: for cell and molecular biology 55, 77–88.
A membrane-bound NAC transcription factor NTL8 regulates gibberellic acid-mediated salt signaling in Arabidopsis seed germination.Crossref | GoogleScholarGoogle Scholar |

Kim HJ, Park JH, Kim J, Kim JJ, Hwang D (2018) Time-evolving genetic networks reveal a NAC troika that negatively regulates leaf senescence in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 115, E4930–E4939.
Time-evolving genetic networks reveal a NAC troika that negatively regulates leaf senescence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29735710PubMed |

Kong CY, Luo YP, Duan TT, Xue Z, Gao XD, Zhao X, Gao G (2016) Potato remorin gene StREMa4 cloning and its spatiotemporal expression pattern under Ralstonia solanacearum and plant hormones treatment. Phytoparasitica 44, 575–584.
Potato remorin gene StREMa4 cloning and its spatiotemporal expression pattern under Ralstonia solanacearum and plant hormones treatment.Crossref | GoogleScholarGoogle Scholar |

Le BN (2004) Fluorescence in situ hybridization (FISH). Current Protocols in Cell Biology 22, 22.4.1–22.4.52.

Lee MH, Jeon HS, Kim HG, Park OK (2017) An Arabidopsis NAC transcription factor NAC4 promotes pathogen induced cell death under negative regulation by microRNA164. New Phytologist 214, 343–360.
An Arabidopsis NAC transcription factor NAC4 promotes pathogen induced cell death under negative regulation by microRNA164.Crossref | GoogleScholarGoogle Scholar | 28032643PubMed |

Lescot M (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.
PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences.Crossref | GoogleScholarGoogle Scholar | 11752327PubMed |

Liang F, Du X, Zhang J, Li XY, Wang F, Wang H, Liu D (2019) Wheat TaLr35PR2 gene is required for Lr35-mediated adult plant resistance against leaf rust fungus. Functional Plant Biology 47, 26–37.
Wheat TaLr35PR2 gene is required for Lr35-mediated adult plant resistance against leaf rust fungus.Crossref | GoogleScholarGoogle Scholar | 31813413PubMed |

López‐Cruz J, Óscar CS, Emma FC, Pilar GA, Carmen GB (2017) Absence of Cu–Zn superoxide dismutase BCSOD1 reduces Botrytis cinerea virulence in Arabidopsis and tomato plants, revealing interplay among reactive oxygen species, callose and signalling pathways. Molecular Plant Pathology 18, 16–31.
Absence of Cu–Zn superoxide dismutase BCSOD1 reduces Botrytis cinerea virulence in Arabidopsis and tomato plants, revealing interplay among reactive oxygen species, callose and signalling pathways.Crossref | GoogleScholarGoogle Scholar | 26780422PubMed |

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.
Callose deposition: a multifaceted plant defense response.Crossref | GoogleScholarGoogle Scholar | 20955078PubMed |

Lv Z, Wang S, Zhang F, Chen L, Hao X, Pan Q (2016) Overexpression of a novel NAC domain-containing transcription factor gene (AaNAC1) enhances the content of artemisinin and increases tolerance to drought and Botrytis cinerea in Artemisia annua. Plant & Cell Physiology 57, 1961–1971.
Overexpression of a novel NAC domain-containing transcription factor gene (AaNAC1) enhances the content of artemisinin and increases tolerance to drought and Botrytis cinerea in Artemisia annua.Crossref | GoogleScholarGoogle Scholar |

Mao H, Yu L, Han R, Li Z, Liu H (2016) ZmNAC55, a maize stress-responsive NAC transcription factor, confers drought resistance in transgenic Arabidopsis. Plant Physiology and Biochemistry 105, 55–66.
ZmNAC55, a maize stress-responsive NAC transcription factor, confers drought resistance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27085597PubMed |

Mao C, Lu S, Lv B, Zhang B, Ming F (2017) A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiology 174, 1747–1763.
A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis.Crossref | GoogleScholarGoogle Scholar | 28500268PubMed |

Murphy F, He Q, Armstrong M, Giuliani LM, Boevink PC, Zhang W (2018) The potato MAP3K StVIK is required for the Phytophthora infestans RXLR effector Pi17316 to promote disease. Plant Physiology 177, 398–410.
The potato MAP3K StVIK is required for the Phytophthora infestans RXLR effector Pi17316 to promote disease.Crossref | GoogleScholarGoogle Scholar | 29588335PubMed |

Na C, Shuanghua W, Jinglong F, Bihao C, Jianjun L, Changming C (2016) Overexpression of the eggplant (Solanum melongena) NAC family transcription factor SmNAC suppresses resistance to bacterial wilt. Scientific Reports 6, 31568
Overexpression of the eggplant (Solanum melongena) NAC family transcription factor SmNAC suppresses resistance to bacterial wilt.Crossref | GoogleScholarGoogle Scholar | 27528282PubMed |

Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi SK (2012) NAC transcription factors in plant abiotic stress responses. BBA - Gene Regulatory Mechanisms 1819, 97–103.
NAC transcription factors in plant abiotic stress responses.Crossref | GoogleScholarGoogle Scholar | 22037288PubMed |

Ni XM, Tian ZD, Liu J, Song BT, Li JC, Shi XL (2010) StPUB17, a novel potato UND/PUB/ARM repeat type gene, is associated with late blight resistance and NaCl stress. Plant Science 178, 158–169.
StPUB17, a novel potato UND/PUB/ARM repeat type gene, is associated with late blight resistance and NaCl stress.Crossref | GoogleScholarGoogle Scholar |

Peeters N, Guidot A, Vailleau F, Valls M (2013) Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Molecular Plant Pathology 14, 651–662.
Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era.Crossref | GoogleScholarGoogle Scholar | 23718203PubMed |

Pimenta MR, Silva PA, Mendes GC, Alves JR, Caetano HDN, Machado JPB (2016) The stress-induced soybean NAC transcription factor GmNAC81 plays a positive role in developmentally programmed leaf senescence. Plant & Cell Physiology 57, 1098–1114.
The stress-induced soybean NAC transcription factor GmNAC81 plays a positive role in developmentally programmed leaf senescence.Crossref | GoogleScholarGoogle Scholar |

Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends in Plant Science 17, 369–381.
NAC proteins: regulation and role in stress tolerance.Crossref | GoogleScholarGoogle Scholar | 22445067PubMed |

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.
Analyzing real-time PCR data by the comparative CT method.Crossref | GoogleScholarGoogle Scholar | 18546601PubMed |

Shan W, Jiane C, Jian-fei K, Wangin L (2015) Banana fruit NAC transcription factor MaNAC5 cooperates with mawrkys to enhance expressions of pathogenesis-related genes against Colletotrichum musae: MaNAC5 cooperates with mawrkys. Molecular Plant Pathology 17, 330–338.
Banana fruit NAC transcription factor MaNAC5 cooperates with mawrkys to enhance expressions of pathogenesis-related genes against Colletotrichum musae: MaNAC5 cooperates with mawrkys.Crossref | GoogleScholarGoogle Scholar | 26033522PubMed |

Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS (2013) Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Research 20, 403–423.
Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.).Crossref | GoogleScholarGoogle Scholar | 23649897PubMed |

Songyikhangsuthor K, Guo Z, Wang N, Zhu X, Xie W, Mou T (2014) Natural variation in the sequence of SNAC1 and its expression level polymorphism in rice germplasms under drought stress. Journal of Genetics and Genomics 41, 609–612.
Natural variation in the sequence of SNAC1 and its expression level polymorphism in rice germplasms under drought stress.Crossref | GoogleScholarGoogle Scholar | 25434685PubMed |

Spoel SH, Dong XN (2012) How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews. Immunology 12, 89–100.
How do plants achieve immunity? Defence without specialized immune cells.Crossref | GoogleScholarGoogle Scholar | 22273771PubMed |

Toth Z, Winterhagen P, Kalapos B, Su Y, Kovacs L, Kiss E (2016) Expression of a grapevine NAC transcription factor gene is induced in response to powdery mildew colonization in salicylic acid-independent manner. Scientific Reports 6, 30825
Expression of a grapevine NAC transcription factor gene is induced in response to powdery mildew colonization in salicylic acid-independent manner.Crossref | GoogleScholarGoogle Scholar | 27488171PubMed |

Turnbull D, Yang L, Naqvi S, Breen S, Welsh L, Stephens J (2017) RXLR effector AVR2 up-regulates a brassinosteroid responsive BHLH transcription factor to suppress immunity. Plant Physiology 174, 356–369.
RXLR effector AVR2 up-regulates a brassinosteroid responsive BHLH transcription factor to suppress immunity.Crossref | GoogleScholarGoogle Scholar | 28270626PubMed |

Wang B, Wei J, Song N, Wang N, Zhao J (2018) A novel wheat NAC transcription factor, TaNAC30, negatively regulates resistance of wheat to stripe rust. Journal of Integrative Plant Biology 60, 432–443.
A novel wheat NAC transcription factor, TaNAC30, negatively regulates resistance of wheat to stripe rust.Crossref | GoogleScholarGoogle Scholar | 29251427PubMed |

Xie Q, Guo HS, Dallman GF, Shengyun W, Allan M, Chua NH (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167–170.
SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals.Crossref | GoogleScholarGoogle Scholar | 12226665PubMed |

Yamaguchi-Shinozaki K, Koizumi M, Urao S, Shinozaki K (1992) Molecular cloning and characterization of 9 CDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: sequence analysis of one CDNA clone that encodes a putative transmembrane channel protein. Plant & Cell Physiology 33, 217–224.
Molecular cloning and characterization of 9 CDNAs for genes that are responsive to desiccation in Arabidopsis thaliana: sequence analysis of one CDNA clone that encodes a putative transmembrane channel protein.Crossref | GoogleScholarGoogle Scholar |

Yang X, He K, Chi X (2018) Miscanthus NAC transcription factor MlNAC12 positively mediates abiotic stress tolerance in transgenic Arabidopsis. Plant Science 277, 229–241.
Miscanthus NAC transcription factor MlNAC12 positively mediates abiotic stress tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30466589PubMed |

Yang XF, Kim MY, Ha J, Lee SH (2019) Overexpression of the soybean NAC Gene GmNAC109 increases lateral root formation and abiotic stress tolerance in transgenic Arabidopsis plants. Plant Science 10, 1036

Zhang L, Yao L, Zhang N, Yang J, Zhu X, Tang X, Calderón-Urrea A, Si H (2018) Lateral root development in potato is mediated by stu-mi164 regulation of NAC transcription factor. Frontiers in Plant Science 9, 383
Lateral root development in potato is mediated by stu-mi164 regulation of NAC transcription factor.Crossref | GoogleScholarGoogle Scholar | 29651294PubMed |

Zhao H, Lou Y, Sun H, Li L, Wang L, Dong L, Gao Z (2016a) Transcriptome and comparative gene expression analysis of Phyllostachys edulis in response to high light. BMC Plant Biology 16, 34
Transcriptome and comparative gene expression analysis of Phyllostachys edulis in response to high light.Crossref | GoogleScholarGoogle Scholar | 26822690PubMed |

Zhao X, Yang X, Pei S, He G, Wang X, Tang Q (2016b) The miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis. Gene 586, 158–169.
The miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27085481PubMed |

Zhong C, Ren Y, Qi Y, Yu X, Wu X, Tian Z (2018) Pamp-responsive ATL gene, StRFP1, and its orthologue, NbATL60, positively regulate, Phytophthora infestans, resistance in potato and Nicotiana benthamiana. Plant Science 270, 47–57.
Pamp-responsive ATL gene, StRFP1, and its orthologue, NbATL60, positively regulate, Phytophthora infestans, resistance in potato and Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 29576086PubMed |