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Citrullus colocynthis NAC transcription factors CcNAC1 and CcNAC2 are involved in light and auxin signaling

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Abstract

Key message

Two novel NAC transcription factors from C itrullus colocynthis implicated in light and auxin signaling pathway.

Abstract

NAC transcription factors (NAM, ATAF1, 2, CUC2) have multiple functions in plant growth and development. Two NACs, CcNAC1 and CcNAC2, were recently identified in the highly drought-tolerant cucurbit species, Citrullus colocynthis. This study examines the functional role of these genes under different qualities of light based on the in silico analysis of the CcNAC1 and CcNAC2 promoters that revealed the presence of several light-associated motifs. The impact of both light and auxin on CcNAC1 and CcNAC2 expression was examined in C. colocynthis leaves, and using reporter (pCcNAC1, 2::GUS) lines in Arabidopsis. Furthermore, the effects of constitutive overexpression (OE-CcNAC1, 2) in Arabidopsis were also examined under a range of conditions to confirm reporter line linkages. White, blue, red, and far-red light treatments resulted in similar patterns of quantitative changes in CcNAC1and CcNAC2 expression in both species, with the highest transcript increases following red light. Photomorphogenic changes in Arabidopsis hypocotyls were correlated with gene transcript levels. In the absence of light, hypocotyls of OE-CcNAC1/CcNAC2 lines were significantly longer as compared to WT. The addition of exogenous auxin (+IAA) to growth medium also resulted in changes to the hypocotyl lengths of overexpression lines and spatiotemporal reporter line changes in seedlings. Our data suggest that CcNAC1, 2 might be functionally important in the light signaling pathway, and appear connected to the hormone auxin. This is the first study to indicate that NAC genes might play a role in both light and auxin signaling pathways.

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Abbreviations

ABA:

Abscisic acid

B:

Blue light

Cc :

Citrullus colocynthis

cry:

Cryptochrome

FR:

Far-red light

GUS:

Beta-d-glucuronidase

IAA:

Indole-3-acetic acid

4-MU:

4-Methylumbelliferone

NAC:

NAM (No apical meristem), ATAF1, 2 (Arabidopsis thaliana activating factor 1, 2), CUC (no apical meristem)

OE:

Overexpression

Phy:

Phytochrome

PIFs:

Phytochrome-interacting factors

Pfr:

Far-red light-absorbing form

Pr:

Red light-absorbing form

R:

Red light

qRT-PCR:

Quantitative real-time polymerase chain reaction

WT:

Wild type

References

  • Altamura MM, Archilletti T, Capone I, Costantino P (1991) Histological analysis of the expression of Agrobacterium rhizogenes rolB-GUS gene fusions in transgenic tobacco. New Phytol 118:69–78

    Article  CAS  Google Scholar 

  • Ang LH, Chattopadhyay S, Wei N, Oyama T, Okada K, Batschauer A, Deng XW (1998) Molecular interactions between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell 1:213–222

    Article  PubMed  CAS  Google Scholar 

  • Argüello-Astorga CR, Herrera-Estrella LR (1996) Ancestral multipartite units in light-responsive plant promoters have structural features correlating with specific phototransduction pathways. Plant Physiol 112:1151–1166

    Article  PubMed  PubMed Central  Google Scholar 

  • Bhatia S, Gangappa SN, Kuswaha R, Kundu S, Chattopadhyay S (2008) SHORT HYPOCOTYL IN WHITE LIGHT1 SHW1, a serine-arginine-aspartate-rich protein in Arabidopsis, acts as a negative regulator of photomorphogenic growth. Plant Physiol 147:169–178

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Briggs WR, Huala E (1999) Blue-light photoreceptors in higher plants. Annu Rev Cell Dev Biol 15:33–62

    Article  PubMed  CAS  Google Scholar 

  • Castelian M, Le Hir R, Bellini C (2012) The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis. Physiol Plant 145:450–460

    Article  Google Scholar 

  • Chae K, Isaacs CG, Reeves PH, Maloney G, Muday GK, Nagpal P, Reed JW (2012) Arabidopsis SMALL AUXIN UP RNA63 promotes hypocotyl and stamen filament elongation. Plant J 71:684–697

    Article  PubMed  CAS  Google Scholar 

  • Chan CS, Guo L, Shih MC (2001) Promoter analysis of the nuclear gene encoding the chloroplast glyceraldehyde-3-phosphate dehydrogenase B subunit of Arabidopsis thaliana. Plant Mol Biol 46:131–141

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee M, Banerjee AK, Hannapel DJ (2007) A BELL1-Like gene of potato is light activated and wound inducible. Plant Physiol 145:1435–1443

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chattopadhyay S, Ang LH, Puente P, Deng XW, Wei N (1998) Arabidopsis bZIP protein HY5 directly interacts with light-responsive promoters in mediating light control of gene expression. Plant Cell 10:673–683

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chen M, Chory J, Fankhauser C (2004) Light signal transduction in higher plants. Annu Rev Genet 38:87–117

    Article  PubMed  CAS  Google Scholar 

  • Cho JN, Ryu JY, Jeong YM, Park J, Song JJ, Amasino RM, Noh B, Noh YS (2012) Control of seed germination by light-induced histone arginine demethylation activity. Dev Cell 22:736–748

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip, a simplified method from agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  Google Scholar 

  • Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38:332–347

    Article  PubMed  CAS  Google Scholar 

  • Colón-Carmona A, Chen DL, Yeh K-C, Abel S (2000) Aux/IAA proteins are phosphorylated by phytochrome in vitro. Plant Physiol 124:1728–1738

    Article  PubMed  PubMed Central  Google Scholar 

  • Dehesh K, Bruce WB, Quail PH (1990) A trans-acting factor that binds to a GF-motif in the phytochrome gene promoter. Science 250:1397–1399

    Article  PubMed  CAS  Google Scholar 

  • Donald RGK, Cashmore AR (1990) Mutation in either G box or I box sequences profoundly affects expression from the Arabidopsis thaliana rbcs-1 A promoter. EMBO J 9:17–26

    Google Scholar 

  • Feldbrugge M, Sprenger M, Dinkelbach M, Yazaki K, Harter K, Weisshaar B (1994) Functional analysis of a light-responsive plant bZIP transcriptional regulator. Plant Cell 6:1607–1621

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Folta FM, Koss LL, McMorrow R, Kim HH, Kenitz D, Wheeler R, Sager JC (2005) Design and fabrication of adjustable red-green-blue LED light arrays for plant research. BMC Plant Biol 5:17–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Gangappa SN, Maurya JP, Yadav V, Chattopadhyay S (2013) The regulation of the Z- and G-box containing promoters by light signaling components, SPA1 and MYC2, in Arabidopsis. PLoS One 8:e62194

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Genoud T, Buchala AJ, Chua NH, Métraux JP (2002) Phytochrome signaling modulates the SA-perceptive pathway in Arabidopsis. Plant J 31:87–95

    Article  PubMed  CAS  Google Scholar 

  • He XJ, Mu RL, Cao WH, Zhang ZG, Zhang JS, Chen SY (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916

    Article  PubMed  CAS  Google Scholar 

  • Ibarra SE, Auge G, Sánchez RA, Botto JF (2013) Transcriptional programs related to phytochrome A function in Arabidopsis seed germination. Mol Plant 6:1261–1273

    Article  PubMed  CAS  Google Scholar 

  • Inoue S, Kinoshita T, Takemiya A, Doi M, Shimazaki K (2008) Leaf positioning of Arabidopsis in responses to blue light. Mol Plant 1:15–26

    Article  PubMed  CAS  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusion, β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed  CAS  PubMed Central  Google Scholar 

  • Jia KP, Luo Q, He SB, Lue XD, Yang HQ (2013) Strigolactone-regulated hypocotyl elongation is dependent on cryptochrome and phytochrome signaling pathways in Arabidopsis. Mol Plant. doi:10.1093/mp/sst093

    Google Scholar 

  • Kanyuka K, Praekelt U, Franklin KA, Billingham OE, Hooley R, Whitelam GC, Halliday KJ (2003) Mutations in the huge Arabidopsis gene BIG affect a range of hormone and light responses. Plant J 35:57–70

    Article  PubMed  CAS  Google Scholar 

  • Kaplan-Levy RN, Brewer PB, Quon T, Smyth DR (2011) The trihelix family of transcription factors-light, stress and development. Trends Plant Sci 17:163–171

    Article  Google Scholar 

  • Kim BC, Soh MS, Hong SH, Furuya M, Nam HG (1998) Photomorphogenic development of the Arabidopsis shy2-1D mutation and its interaction with phytochromes in darkness. Plant J 15:61–68

    Article  PubMed  CAS  Google Scholar 

  • Kimura M, Yamamoto YY, Seki M, Sakarai T, Sato M, Abe T, Yoshida S, Manabe K, Shinozaki K, Matsui M (2003) Identification of Arabidopsis genes regulated by high light-stress using cDNA microarray. Photochem Photobiol Sci 77:226–233

    CAS  Google Scholar 

  • Koornneef M, Rolff E, Spruit CIP (1980) Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana. Z Pflanzenphysiol 100:147–160

    Article  Google Scholar 

  • Kraepiel Y, Miginiac E (1997) Photomorphogenesis and phytohormones. Plant Cell Environ 20:807–812

    Article  CAS  Google Scholar 

  • Kuhn RM, Caspar T, Dehesh K, Quail PH (1993) DNA binding factor GT-2 from Arabidopsis. Plant Mol Biol 23:337–348

    Article  PubMed  CAS  Google Scholar 

  • Kurepin LV, Walton LJ, Reid DM, Chinnappa C (2010) Light regulation of endogenous salicylic acid levels in hypocotyls of Helianthus annuus seedlings. Botany 88:668–674

    Article  CAS  Google Scholar 

  • Lau OS, Deng XW (2010) Plant hormone signaling lightens up, integrators of light and hormone. Curr Opin Plant Biol 13:571–577

    Article  PubMed  CAS  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé 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 Res 1:325–327

    Article  Google Scholar 

  • Lin R, Wang H (2005) Two homologous ATP-Binging cassette transporter protein, AtMDR1 and AtPGP1, regulate Arabidopsis photomorphogenesis and root development by mediating polar auxin transport. Plant Physiol 138:949–964

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lin JF, Wu SH (2004) Molecular events in senescing Arabidopsis leaves. Plant J 39:612–628

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Cohen JD, Gardner G (2011) Low-fluence red light increases the transport and biosynthesis of auxin. Plant Physiol 157:891–904

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Millenaar FF, van Zanten M, Cox MCH, Pierik R, Voesenek LACJ, Peeters AJM (2009) Differential petiole growth in Arabidopsis thaliana, photocontrol and hormonal regulation. New Phytol 184:141–152

    Article  PubMed  CAS  Google Scholar 

  • Monte E, Al-Sady B, Leivar P, Quail PH (2007) Out of the dark, how the PIFs are unmasking a dual temporal mechanism of phytochrome signaling. J Exp Bot 58:3125–3133

    Article  PubMed  CAS  Google Scholar 

  • Morishita T, Kojima Y, Maruta T, Nishizawa-Yokoi A, Yabuta Y, Shigeoka S (2009) Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high light. Plant Cell Physiol 50:2210–2222

    Article  PubMed  CAS  Google Scholar 

  • Nagpal P, Walker LM, Yong JC, Sonawala A, Timpte C, Estelle M, Reed JW (2000) AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123:563–573

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Nalbandi K, Kohnehrouz BB, Saeed KA, Gholizadeh A (2012) Isolating barley Hordeum vulgare L. B1 hordein gene promoter and using sequencing analysis for the identification of conserved regulatory elements by bioinformatics tools. Afr J Biotechnol 11:7378–7387

    CAS  Google Scholar 

  • Nusinow DA, Helfer A, Hamilton EE, King JJ, Imaizumi T, Schultz TF, Farré EM, Kay SA (2011) The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors, structurally distinct, functionally diverse. Trends Plant Sci 10:79–87

    Article  PubMed  CAS  Google Scholar 

  • Oyama T, Shimura Y, Okada K (1997) The Arabidopsis HY5 gene encodes a b ZIP protein that regulates stimulus-induced development of root and hypocotyl. Genes Dev 11:2983–2995

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Park SC, Kwon HB, Shih MC (1996) Cis-acting elements essential for light regulation of the nuclear gene encoding the A subunit of chloroplast glyceraldehyde 3-phosphate dehydrogenase in Arabidopsis thaliana. Plant Physiol 112:1563–1571

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Park J, Kim YS, Kim SG, Jung JH, Woo JC, Park CM (2011) Integration of auxin and salt signals by the NAC transcription factor NTM2 during seed germination in Arabidopsis. Plant Physiol 156:537–549

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Parks BM (2003) The red side of photomorphogenesis. Plant Physiol 33:1437–1444

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. NAR 29:e45

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Poppenberger B, Fujioka S, Soeno K, Soeno K, George GL, Vaistij FE, Hiranuma S, Seto H, Takatsuto S, Adam G, Yoshida S, Bowles D (2005) The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. PNAS 102:15253–15258

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Rajendra V, Prasad B, Kumar SV, Nandi A, Chattopadhyay S (2012) Functional interconnections of HY1 with MYC2 and HY5 in Arabidopsis seedling development. BMC Plant Biol 12:37–50

    Article  Google Scholar 

  • Rizzini L, Favory J-J, Cloix C, Faggionato D, O’Hara A, Kaiserli E, Baumeister R, Schäfer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 Protein. Science 332:103–106

    Article  PubMed  CAS  Google Scholar 

  • Romano CP, Robson PR, Smith H, Estelle M, Klee H (1995) Transgene-mediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resistant mutants. Plant Mol Biol 27:1071–1083

    Article  PubMed  CAS  Google Scholar 

  • Safrany J, Haasz V, Mate Z, Ciolfi A, Feher B, Oravecz A, Stec A, Dallmann G, Morelli G, Ulm R, Nagy F (2008) Identification of a novel cis-regulatory element for UV-B-induced transcription in Arabidopsis. Plant J 54:402–414

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Watahiki MK, Yamamoto KT (2007) Differential expression of the auxin primary response gene MASSUGU2/IAA19 during tropic responses of Arabidopsis hypocotyls. Physiol Plant 130:148–156

    Article  CAS  Google Scholar 

  • Shikata H, Shibata M, Ushijima T, Nakashima M, Kong SG, Matsuoka K, Lin C, Matsushita T (2012) The RS domain of Arabidopsis splicing factor RRC1 is required for phytochrome B signal transduction. Plant J 70:727–738

    Article  PubMed  CAS  Google Scholar 

  • Smirnova OG, Stepanenko IL, Shumny VK (2012) Mechanism of action and activity regulation of COP1, a constitutive repressor of photomorphogenesis. Russ J Plant Physl 59:155–166

    Article  CAS  Google Scholar 

  • Song YH, Yoo CM, Hong AP, Kim SH, Jeong HJ, Shin SY, Kim HJ, Yun DJ, Lim CO, Bahk JD, Lee SY, Nagao RT, Key JL, Hong JC (2008) DNA-binding study identifies C-box and hybrid C/G-box or C/A-box motifs as high-affinity binding sites for STF1 and LONG HYPOCOTYL5 proteins. Plant Physiol 146:1862–1877

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sorce C, Picciarelli P, Calistri G, Lercari B, Ceccarelli N (2008) The involvement of indole-3-acetic acid in the control of stem elongation in dark- and light-grown pea Pisum sativum. seedlings. J Plant Physiol 165:482–489

    Article  PubMed  CAS  Google Scholar 

  • Soy J, Leivar P, González-Schain N, Sentandreu M, Prat S, Quail PH, Monte E (2012) Phytochrome-imposed oscillations in PIF3 protein abundance regulate hypocotyl growth under diurnal light/dark conditions in Arabidopsis. Plant J 71:390–401

    PubMed  CAS  PubMed Central  Google Scholar 

  • Sun J, Qi L, Li Y, Zhai Q, Li C (2013) PIF4 and PIF5 transcription factors link blue light and auxin to regulate the phototropic response in Arabidopsis. Plant Cell. doi:10.1105/tpc.113.112417

    Google Scholar 

  • Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46:445–474

    Article  CAS  Google Scholar 

  • Thanh T, Chi VTQ, Omar H, Abdullah MP, Napis S (2012) Sequence analysis and potentials of the native Rbcs promoter in the development of an alternative eukaryotic expression system using green microalga Ankistrodesmus convolutus. Int J Mol Sci 13:2676–2691

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tian Q, Reed J (2001) Molecular links between light and auxin signalling pathways. Plant Growth Regul 20:274–280

    Article  CAS  Google Scholar 

  • Ulm R, Baumann A, Oravecz A, Máté Z, Adám E, Oakeley EJ, Schäfer E, Nagy F (2004) Genome-wide analysis of gene expression reveals function of the bZIP transcription factor HY5 in the UV-B response of Arabidopsis. PNAS 101:1397–1402

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Valdés AE, Rizzardi K, Johannnesson H, Para A, Sundås-larsson A, Landberg K (2012) Arabidopsis thaliana TERMINAL FLOWER2 is involved in light-controlled signaling during seedling photomorphogenesis. Plant, Cell Environ 5:1013–1025

    Article  Google Scholar 

  • Vanderbussche F, Pierik R, Millenaar FF, Voesenek LA, Van Der Straeten D (2005) Reaching out of the shade. Curr Opin Plant Boil 8:462–468

    Article  Google Scholar 

  • Viret JF, Mabrouk Y, Bogorad L (1994) Transcriptional photoregulation of celltype preferred expression of maize rbcSm3, 3′ and 5′ sequences are involved. PNAS 91:8577–8581

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang Z, Dane F (2013) NAC (NAM/ATAF/CUC) transcription factors in different stresses and their signaling pathway. Acta Physiol Plant 35:1397–1408

    Article  CAS  Google Scholar 

  • Wang R, Hong G, Han B (2004) Transcript abundance of rml1, encoding a putative GT1-like factor in rice, is up-regulated by Magnaporthe grisea and down-regulated by light. Gene 324:105–115

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Li L, Xu L, Zhou J, Zhuang H, Gong X, Wang M, Samuel SMS, Zhuge Q (2013) Isolation and functional analysis of the poplar RbcS gene promoter. Plant Mol Biol Rep 13:120–127

    Article  Google Scholar 

  • Wang Z, Rashotte A, Moss AG, Dane F (2014) Two NAC transcription factors from Citrullus colocynthis, CcNAC1, CcNAC2 implicated in multiple stress response. Acta Physiol Plant 36:621–634

    Article  Google Scholar 

  • Wu G, Cameron JN, Ljung K, Spalding EP (2010) A role for ABCB19-mediated polar auxin transport in seedling photomorphogenesis mediated by cryptochrome1 and phytochrome B. Plant J 62:179–191

    Article  PubMed  CAS  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chun NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yamada T, Tanaka Y, Sriprasertsak P, Kato H, Hashimoto T, Shimizu H, Shiraushi T (1992) Phenylalanine ammonia-lyase genes from Pisum sativum, structure, organ specific expression and regulation by funga1 elicitor and suppressor. Plant Cell Physiol 33:715–725

    CAS  Google Scholar 

  • Zhang H, He H, Wang X, Wang X, Yang X, Li L, Deng XW (2011) Genome-wide mapping of the HY5-mediated gene networks in Arabidopsis that involve both transcriptional and post-transcriptional regulation. Plant J 65:346–358

    Article  PubMed  CAS  Google Scholar 

  • Zhou DX (1999) Regulatory mechanism of plant gene transcription by GT-elements and GT-factors. Trends Plant Sci 4:201–214

    Article  Google Scholar 

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Acknowledgments

We gratefully acknowledge the support of Dr. Kevin M. Folta from Florida State University for the R, FR and B light treatment equipment.

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  1. Department of Horticulture, Auburn University, Auburn, AL, 36849, USA

    Zhuoyu Wang & Fenny Dane

  2. Department of Biological Sciences, Auburn University, Auburn, AL, 36849, USA

    Aaron M. Rashotte

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  1. Zhuoyu Wang
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Correspondence to Fenny Dane.

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Communicated by Ying-Tang Lu.

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Wang, Z., Rashotte, A.M. & Dane, F. Citrullus colocynthis NAC transcription factors CcNAC1 and CcNAC2 are involved in light and auxin signaling. Plant Cell Rep 33, 1673–1686 (2014). https://doi.org/10.1007/s00299-014-1646-z

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