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

PaNAC089 is a membrane-tethered transcription factor (MTTF) that modulates flowering, chlorophyll breakdown and trichome initiation

Changsheng Shao https://orcid.org/0000-0002-9078-0551 A , Fangfang Cai A B , Zhiru Bao A , Yanping Zhang A , Gehui Shi A , Zheng Zhou A , Xiyan Chen A , Yangyang Li A , Manzhu Bao A * and Jiaqi Zhang A *
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, Hubei, China.

B Plant Genomics & Molecular Improvement of Colored Fiber Laboratory, College of Life Sciences and Medicine, Zhejiang Sci-Tech University, Hangzhou 310018, Zhejiang, China.


Handling Editor: Ulrike Mathesius

Functional Plant Biology 49(4) 392-404 https://doi.org/10.1071/FP21320
Submitted: 26 October 2021  Accepted: 31 January 2022   Published: 25 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Flowering and senescence are essential developmental stages of green plants, which are governed by complex molecular regulatory networks. However, the connection between flowering regulation and senescence regulation in London plane tree (Platanus acerifolia) remains unknown. In this study, we identified a gene PaNAC089 from London plane tree, which encodes a membrane-tethered transcription factor (MTTF) belonging to the NAC (NAM, ATAF1/2, CUC2) transcription factor family. We investigated the functions of PaNAC089 in the regulation of flowering and senescence through the analysis of expression profiles and transgenic phenotypes. Heterologous overexpression of ΔPaNAC089 delayed flowering and inhibited chlorophyll breakdown to produce dark green rosette leaves in Arabidopsis. In addition, the trichome density of rosette leaves was decreased in transgenic lines. In ΔPaNAC089 overexpression plants, a series of functional genes with inhibited expression were identified by quantitative real-time polymerase chain reaction (qRT-PCR), including genes that regulate flowering, chlorophyll decomposition, and trichome initiation. Furthermore, ΔPaNAC089 directly binds to the promoter of CONSTANS (CO) and NON-YELLOWING2 (NYE2) in the yeast one-hybrid assay. Consistent with this, luciferase (LUC) transient expression assays also showed that ΔPaNAC089 could inhibit the activity of NYE2. To summarise, our data suggests that PaNAC089 is an MTTF that modulates flowering, chlorophyll breakdown and trichome initiation.

Keywords: ΔPaNAC089, Chl breakdown, delays flowering, MTTFs, NAC TFs, PaNAC089, Platanus acerifolia, trichomes.


References

Albertos P, Tatematsu K, Mateos I, Sánchez-Vicente I, Fernández-Arbaizar A, Nakabayashi K, Nambara E, Godoy M, Franco JM, Solano R, Gerna D, Roach T, Stöggl W, Kranner I, Perea-Resa C, Salinas J, Lorenzo O (2021) Redox feedback regulation of ANAC089 signaling alters seed germination and stress response. Cell Reports 35, 109263
Redox feedback regulation of ANAC089 signaling alters seed germination and stress response.Crossref | GoogleScholarGoogle Scholar | 34133931PubMed |

Bai M, Sun J, Liu J, Ren H, Wang K, Wang Y, Wang C, Dehesh K (2019) The B-box protein BBX19 suppresses seed germination via induction of ABI5. The Plant Journal 99, 1192–1202.
The B-box protein BBX19 suppresses seed germination via induction of ABI5.Crossref | GoogleScholarGoogle Scholar | 31112314PubMed |

Bar M, Shtein I (2019) Plant trichomes and the biomechanics of defense in various systems, with Solanaceae as a model. Botany 97, 651–660.
Plant trichomes and the biomechanics of defense in various systems, with Solanaceae as a model.Crossref | GoogleScholarGoogle Scholar |

Chen J, Zhu X, Ren J, Qiu K, Li Z, Xie Z, Gao J, Zhou X, Kuai B (2017) Suppressor of overexpression of CO 1 negatively regulates dark-induced leaf degreening and senescence by directly repressing pheophytinase and other senescence-associated genes in arabidopsis. Plant Physiology 173, 1881–1891.
Suppressor of overexpression of CO 1 negatively regulates dark-induced leaf degreening and senescence by directly repressing pheophytinase and other senescence-associated genes in arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28096189PubMed |

Christ B, Hörtensteiner S (2014) Mechanism and significance of chlorophyll breakdown. Journal of Plant Growth Regulation 33, 4–20.
Mechanism and significance of chlorophyll breakdown.Crossref | GoogleScholarGoogle Scholar |

Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 10069079PubMed |

Du S-S, Li L, Li L, Wei X, Xu F, Xu P, Wang W, Xu P, Cao X, Miao L, Guo T, Wang S, Mao Z, Yang H-Q (2020) Photoexcited cryptochrome2 interacts directly with TOE1 and TOE2 in flowering regulation. Plant Physiology 184, 487–505.
Photoexcited cryptochrome2 interacts directly with TOE1 and TOE2 in flowering regulation.Crossref | GoogleScholarGoogle Scholar | 32661061PubMed |

Duval M, Hsieh T-F, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Molecular Biology 50, 237–248.
Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily.Crossref | GoogleScholarGoogle Scholar | 12175016PubMed |

Ernst HA, Olsen AN, Larsen S, Lo Leggio L (2004) Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors. EMBO Reports 5, 297–303.
Structure of the conserved domain of ANAC, a member of the NAC family of transcription factors.Crossref | GoogleScholarGoogle Scholar | 15083810PubMed |

Fujiwara S, Mitsuda N (2016) ANAC075, a putative regulator of VASCULAR-RELATED NAC-DOMAIN7, is a repressor of flowering. Plant Biotechnology 33, 255–265.
ANAC075, a putative regulator of VASCULAR-RELATED NAC-DOMAIN7, is a repressor of flowering.Crossref | GoogleScholarGoogle Scholar | 31367182PubMed |

Gan Y, Liu C, Yu H, Broun P (2007) Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 134, 2073–2081.
Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate.Crossref | GoogleScholarGoogle Scholar | 17507408PubMed |

Gao S, Gao J, Zhu X, Song Y, Li Z, Ren G, Zhou X, Kuai B (2016) ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in arabidopsis. Molecular Plant 9, 1272–1285.
ABF2, ABF3, and ABF4 promote ABA-mediated chlorophyll degradation and leaf senescence by transcriptional activation of chlorophyll catabolic genes and senescence-associated genes in arabidopsis.Crossref | GoogleScholarGoogle Scholar | 27373216PubMed |

Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C (2010) Senescence and death of plant organs: nutrient recycling and developmental regulation. Comptes Rendus Biologies 333, 382–391.
Senescence and death of plant organs: nutrient recycling and developmental regulation.Crossref | GoogleScholarGoogle Scholar | 20371113PubMed |

Guo S, Dai S, Singh PK, Wang H, Wang Y, Tan JLH, Wee W, Ito T (2018) A membrane-bound NAC-Like transcription factor OsNTL5 represses the flowering in Oryza sativa. Frontiers in Plant Science 9, 555
A membrane-bound NAC-Like transcription factor OsNTL5 represses the flowering in Oryza sativa.Crossref | GoogleScholarGoogle Scholar | 29774039PubMed |

Huang B, Qian P, Gao N, Shen J, Hou S (2017) Fackel interacts with gibberellic acid signaling and vernalization to mediate flowering in Arabidopsis. Planta 245, 939–950.
Fackel interacts with gibberellic acid signaling and vernalization to mediate flowering in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28108812PubMed |

Irani H, ValizadehKaji B, Naeini MR (2021) Biostimulant-induced drought tolerance in grapevine is associated with physiological and biochemical changes. Chemical and Biological Technologies in Agriculture 8, 5
Biostimulant-induced drought tolerance in grapevine is associated with physiological and biochemical changes.Crossref | GoogleScholarGoogle Scholar |

Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P (2019) Protective and defensive roles of non-glandular trichomes against multiple stresses: structure–function coordination. Journal of Forestry Research 31, 1–12.
Protective and defensive roles of non-glandular trichomes against multiple stresses: structure–function coordination.Crossref | GoogleScholarGoogle Scholar |

Kikuchi K, Ueguchi-Tanaka M, Yoshida KT, Nagato Y, Matsusoka M, Hirano HY (2000) Molecular analysis of the NAC gene family in rice. Molecular and General Genetics MGG 262, 1047–1051.
Molecular analysis of the NAC gene family in rice.Crossref | GoogleScholarGoogle Scholar | 10660065PubMed |

Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH, Phee BK, Rupak T, Jeong H, Lee Y, Hong BS, Nam HG, Woo HR, Lim PO (2014) Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. Journal of Experimental Botany 65, 4023–4036.
Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 24659488PubMed |

Klein P, Seidel T, Stöecker B, Dietz K-J (2012) The membrane-tethered transcription factor ANAC089 serves as redox-dependent suppressor of stromal ascorbate peroxidase gene expression. Frontiers in Plant Science 3, 247
The membrane-tethered transcription factor ANAC089 serves as redox-dependent suppressor of stromal ascorbate peroxidase gene expression.Crossref | GoogleScholarGoogle Scholar | 23162559PubMed |

Kuai B, Chen J, Hörtensteiner S (2018) The biochemistry and molecular biology of chlorophyll breakdown. Journal of Experimental Botany 69, 751–767.
The biochemistry and molecular biology of chlorophyll breakdown.Crossref | GoogleScholarGoogle Scholar | 28992212PubMed |

Kumar A, Singh A, Panigrahy M, Sahoo PK, Panigrahi KCS (2018) Carbon nanoparticles influence photomorphogenesis and flowering time in Arabidopsis thaliana. Plant Cell Reports 37, 901–912.
Carbon nanoparticles influence photomorphogenesis and flowering time in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Li Z, Liu G, Zhang J, Zhang J, Bao M (2008) Extraction of high-quality tissue-specific RNA from London plane trees (Platanus acerifolia), permitting the construction of a female inflorescence cDNA library. Functional Plant Biology 35, 159–165.
Extraction of high-quality tissue-specific RNA from London plane trees (Platanus acerifolia), permitting the construction of a female inflorescence cDNA library.Crossref | GoogleScholarGoogle Scholar | 32688767PubMed |

Li J, Zhang J, Wang X, Chen J (2010) A membrane-tethered transcription factor ANAC089 negatively regulates floral initiation in Arabidopsis thaliana. Science China-Life Sciences 53, 1299–1306.
A membrane-tethered transcription factor ANAC089 negatively regulates floral initiation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 21046321PubMed |

Li S, Gao J, Yao L, Ren G, Zhu X, Gao S, Qiu K, Zhou X, Kuai B (2016) The role of ANAC072 in the regulation of chlorophyll degradation during age- and dark-induced leaf senescence. Plant Cell Reports 35, 1729–1741.
The role of ANAC072 in the regulation of chlorophyll degradation during age- and dark-induced leaf senescence.Crossref | GoogleScholarGoogle Scholar | 27154758PubMed |

Li Z, Wu S, Chen J, Wang X, Gao J, Ren G, Kuai B (2017) NYEs/SGRs-mediated chlorophyll degradation is critical for detoxification during seed maturation in Arabidopsis. The Plant Journal 92, 650–661.
NYEs/SGRs-mediated chlorophyll degradation is critical for detoxification during seed maturation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28873256PubMed |

Liang M, Li H, Zhou F, Li H, Liu J, Hao Y, Wang Y, Zhao H, Han S (2015) Subcellular Distribution of NTL Transcription Factors in Arabidopsis thaliana. Traffic 16, 1062–1074.
Subcellular Distribution of NTL Transcription Factors in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 26201836PubMed |

Liu S, Qi T, Ma J, Ma T, Ma L, Lin X (2016) Ectopic expression of a SOC1 homolog from Phyllostachys violascens alters flowering time and identity of floral organs in Arabidopsis thaliana. Trees 30, 2203–2215.
Ectopic expression of a SOC1 homolog from Phyllostachys violascens alters flowering time and identity of floral organs in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Liu Y, Liu D, Khan AR, Liu B, Wu M, Huang L, Wu J, Song G, Ni H, Ying H, Yu H, Gan Y (2018) NbGIS regulates glandular trichome initiation through GA signaling in tobacco. Plant Molecular Biology 98, 153–167.
NbGIS regulates glandular trichome initiation through GA signaling in tobacco.Crossref | GoogleScholarGoogle Scholar | 30171399PubMed |

Long Y, Schiefelbein J (2020) Novel TTG1 mutants modify root-hair pattern formation in Arabidopsis. Frontiers in Plant Science 11, 383
Novel TTG1 mutants modify root-hair pattern formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 32318087PubMed |

Lu S, Li Z, Zhang J, Yi S, Liu L, Bao M, Liu G (2012) Isolation and expression analysis of a LEAFY/FLORICAULA homolog and its promoter from London plane (Platanus acerifolia Willd.). Plant Cell Reports 31, 1851–1865.
Isolation and expression analysis of a LEAFY/FLORICAULA homolog and its promoter from London plane (Platanus acerifolia Willd.).Crossref | GoogleScholarGoogle Scholar | 22821362PubMed |

Lu J, Bai M, Ren H, Liu J, Wang C (2017) An efficient transient expression system for gene function analysis in rose. Plant Methods 13, 116
An efficient transient expression system for gene function analysis in rose.Crossref | GoogleScholarGoogle Scholar | 29299050PubMed |

Monniaux M, McKim SM, Cartolano M, Thévenon E, Parcy F, Tsiantis M, Hay A (2017) Conservation vs divergence in LEAFY and APETALA1 functions between Arabidopsis thaliana and Cardamine hirsuta. New Phytologist 216, 549–561.
Conservation vs divergence in LEAFY and APETALA1 functions between Arabidopsis thaliana and Cardamine hirsuta.Crossref | GoogleScholarGoogle Scholar |

Pesch M, Schultheiß I, Klopffleisch K, Uhrig JF, Koegl M, Clemen CS, Simon R, Weidtkamp-Peters S, Hülskamp M (2015) TRANSPARENT TESTA GLABRA1 and GLABRA1 compete for binding to GLABRA3 in Arabidopsis. Plant Physiology 168, 584–597.
TRANSPARENT TESTA GLABRA1 and GLABRA1 compete for binding to GLABRA3 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 25926482PubMed |

Sakuraba Y, Han S-H, Lee S-H, Höertensteiner S, Paek N-C (2016) Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription. Plant Cell Reports 35, 155–166.
Arabidopsis NAC016 promotes chlorophyll breakdown by directly upregulating STAYGREEN1 transcription.Crossref | GoogleScholarGoogle Scholar | 26441053PubMed |

Schellmann S, Hulskamp M (2005) Epidermal differentiation: trichomes in Arabidopsis as a model system. The International Journal of Developmental Biology 49, 579–584.
Epidermal differentiation: trichomes in Arabidopsis as a model system.Crossref | GoogleScholarGoogle Scholar | 16096966PubMed |

Shim JS, Kubota A, Imaizumi T (2017) Circadian clock and photoperiodic flowering in Arabidopsis: CONSTANS is a hub for signal integration. Plant Physiology 173, 5–15.
Circadian clock and photoperiodic flowering in Arabidopsis: CONSTANS is a hub for signal integration.Crossref | GoogleScholarGoogle Scholar | 27688622PubMed |

Shimoda Y, Ito H, Tanaka A (2016) Arabidopsis STAY-GREEN, mendel’s green cotyledon gene, encodes magnesium-dechelatase. Plant Cell 28, 2147–2160.
Arabidopsis STAY-GREEN, mendel’s green cotyledon gene, encodes magnesium-dechelatase.Crossref | GoogleScholarGoogle Scholar | 27604697PubMed |

Slabaugh E, Brandizzi F (2011) Membrane-tethered transcription factors provide a connection between stress response and developmental pathways. Plant Signaling & Behavior 6, 1210–1211.
Membrane-tethered transcription factors provide a connection between stress response and developmental pathways.Crossref | GoogleScholarGoogle Scholar |

Sukiran NL, Ma JC, Ma H, Su Z (2019) ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis. Plant Molecular Biology 99, 161–174.
ANAC019 is required for recovery of reproductive development under drought stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 30604322PubMed |

Tian H, Wang X, Guo H, Cheng Y, Hou C, Chen J-G, Wang S (2017) NTL8 regulates trichome formation in Arabidopsis by directly activating R3 MYB Genes TRY and TCL1. Plant Physiology 174, 2363–2375.
NTL8 regulates trichome formation in Arabidopsis by directly activating R3 MYB Genes TRY and TCL1.Crossref | GoogleScholarGoogle Scholar | 28649093PubMed |

Tran L-SP, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. The Plant Cell 16, 2481–2498.
Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter.Crossref | GoogleScholarGoogle Scholar |

Wang XL, Gao J, Gao S, Song Y, Yang Z, Kuai BK (2019a) The H3K27me3 demethylase REF6 promotes leaf senescence through directly activating major senescence regulatory and functional genes in Arabidopsis. PLoS Genetics 15, e1008068
The H3K27me3 demethylase REF6 promotes leaf senescence through directly activating major senescence regulatory and functional genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Wang Z, Yang Z, Li F (2019b) Updates on molecular mechanisms in the development of branched trichome in Arabidopsis and nonbranched in cotton. Plant Biotechnology Journal 17, 1706–1722.
Updates on molecular mechanisms in the development of branched trichome in Arabidopsis and nonbranched in cotton.Crossref | GoogleScholarGoogle Scholar | 31111642PubMed |

Wang M-J, Ding L, Liu X-H, Liu J-X (2021) Two B-box domain proteins, BBX28 and BBX29, regulate flowering time at low ambient temperature in Arabidopsis. Plant Molecular Biology 106, 21–32.
Two B-box domain proteins, BBX28 and BBX29, regulate flowering time at low ambient temperature in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 33554307PubMed |

Wu S, Li Z, Yang L, Xie Z, Chen J, Zhang W, Liu T, Gao S, Gao J, Zhu Y, Xin J, Ren G, Kuai B (2016) NON-YELLOWING2 (NYE2), a Close Paralog of NYE1, plays a positive role in chlorophyll degradation in Arabidopsis. Molecular Plant 9, 624–627.
NON-YELLOWING2 (NYE2), a Close Paralog of NYE1, plays a positive role in chlorophyll degradation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26732493PubMed |

Xie Z, Wu S, Chen J, Zhu X, Zhou X, Hörtensteiner S, Ren G, Kuai B (2019) The C-terminal cysteine-rich motif of NYE1/SGR1 is indispensable for its function in chlorophyll degradation in Arabidopsis. Plant Molecular Biology 101, 257–268.
The C-terminal cysteine-rich motif of NYE1/SGR1 is indispensable for its function in chlorophyll degradation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 31302867PubMed |

Yan J, Chen Q, Cui X, Zhao P, Gao S, Yang B, Liu J-X, Tong T, Deyholos MK, Jiang Y-Q (2021) Ectopic overexpression of a membrane-tethered transcription factor gene NAC60 from oilseed rape positively modulates programmed cell death and age-triggered leaf senescence. The Plant Journal 105, 600–618.
Ectopic overexpression of a membrane-tethered transcription factor gene NAC60 from oilseed rape positively modulates programmed cell death and age-triggered leaf senescence.Crossref | GoogleScholarGoogle Scholar | 33119146PubMed |

Yang Z-T, Wang M-J, Sun L, Lu S-J, Bi D-L, Sun L, Song Z-T, Zhang S-S, Zhou S-F, Liu J-X (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genetics 10, e1004243
The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants.Crossref | GoogleScholarGoogle Scholar | 24675811PubMed |

Yang T, He Y, Niu S, Yan S, Zhang Y (2020) Identification and characterization of the CONSTANS (CO)/CONSTANS-like (COL) genes related to photoperiodic signaling and flowering in tomato. Plant Science 301, 110653
Identification and characterization of the CONSTANS (CO)/CONSTANS-like (COL) genes related to photoperiodic signaling and flowering in tomato.Crossref | GoogleScholarGoogle Scholar | 33218623PubMed |

Yin XR, Xie XL, Xia XJ, Yu JQ, Ferguson IB, Giovannoni JJ, Chen KS (2016) Involvement of an ethylene response factor in chlorophyll degradation during citrus fruit degreening. The Plant Journal 86, 403–412.
Involvement of an ethylene response factor in chlorophyll degradation during citrus fruit degreening.Crossref | GoogleScholarGoogle Scholar | 27037684PubMed |

Zhang H, Cui X, Guo Y, Luo C, Zhang L (2018) Picea wilsonii transcription factor NAC2 enhanced plant tolerance to abiotic stress and participated in RFCP1-regulated flowering time. Plant Molecular Biology 98, 471–493.
Picea wilsonii transcription factor NAC2 enhanced plant tolerance to abiotic stress and participated in RFCP1-regulated flowering time.Crossref | GoogleScholarGoogle Scholar | 30406468PubMed |

Zhang G, Huang S, Zhang C, Li D, Wu Y, Deng J, Shan S, Qi J (2021) Overexpression of CcNAC1 gene promotes early flowering and enhances drought tolerance of jute (Corchorus capsularis L.). Protoplasma 258, 337–345.
Overexpression of CcNAC1 gene promotes early flowering and enhances drought tolerance of jute (Corchorus capsularis L.).Crossref | GoogleScholarGoogle Scholar | 33079225PubMed |

Zhou F-Y, Han Y-J, Wang Y-H, Yao C-C, Zhang Y (2021) Overexpression of Polypogon fugax Type I–Like MADS-Box Gene PfAGL28 affects flowering time and pod formation in transgenic Arabidopsis. Plant Molecular Biology Reporter
Overexpression of Polypogon fugax Type I–Like MADS-Box Gene PfAGL28 affects flowering time and pod formation in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Zhu X, Chen J, Xie Z, Gao J, Ren G, Gao S, Zhou X, Kuai B (2015) Jasmonic acid promotes degreening via MYC2/3/4-and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes. The Plant Journal 84, 597–610.
Jasmonic acid promotes degreening via MYC2/3/4-and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes.Crossref | GoogleScholarGoogle Scholar | 26407000PubMed |