Skip to main content
Log in

Poplar GATA transcription factor PdGNC is capable of regulating chloroplast ultrastructure, photosynthesis, and vegetative growth in Arabidopsis under varying nitrogen levels

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

An Erratum to this article was published on 04 September 2014

Abstract

Photosynthesis and nitrogen availability are crucial to the accumulation of biomass. The GATA transcription factor family plays important roles in chloroplast development and nitrogen metabolism. Here, we cloned, for the first time, the GATA transcription factor PdGNC from the fast-growing poplar clone NE-19. The overexpression results from Arabidopsis under high nitrate, sufficient nitrate, and low nitrate (LN) support that PdGNC increased the chloroplast number and size per cell in leaf and stem, improved the chlorophyll level by 26.12 % and exhibited the highest starch content in LN. Overexpression of PdGNC also had pronounced effects on chloroplast ultrastructure by increasing the number of grana and thylakoids. The photosynthetic rate in transgenic LN lines was 42.17 % higher than in the wild type through modification of the chlorophyll fluorescence parameters Fv/F0, Fv/Fm, qP, NPQ, and ΦPSII. Morphologically, PdGNC promoted longer primary roots and larger leaf areas, and exhibited a higher relative growth rate in LN. Altogether, PdGNC improved photosynthetic capacity and plant growth under low nitrate levels; thus, it could potentially be used in transgenic breeding to improve nitrate utilization and plant growth rates under limited nitrogen conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ariovich D, Cresswell C (1983) The effect of nitrogen and phosphorus on starch accumulation and net photosynthesis in two variants of Panicum maximum Jacq. Plant Cell Environ 6(8):657–664

    Article  CAS  Google Scholar 

  • Armstrong GA, Runge S, Frick G, Sperling U, Apel K (1995) Identification of NADPH:protochlorophyllide oxidoreductases A and B: a branched pathway for light-dependent chlorophyll biosynthesis in Arabidopsis thaliana. Plant Physiol 108(4):1505–1517

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55(403):1607–1621. doi:10.1093/Jxb/Erh196

    Article  PubMed  CAS  Google Scholar 

  • Bechtold N, Jolivet S, Voisin R, Pelletier G (2003) The endosperm and the embryo of Arabidopsis thaliana are independently transformed through infiltration by Agrobacterium tumefaciens. Transgenic Res 12(4):509–517. doi:10.1023/A:1024272023966

    Article  PubMed  CAS  Google Scholar 

  • Bi YM, Zhang Y, Signorelli T, Zhao R, Zhu T, Rothstein S (2005) Genetic analysis of Arabidopsis GATA transcription factor gene family reveals a nitrate-inducible member important for chlorophyll synthesis and glucose sensitivity. Plant J Cell Mol Biol 44(4):680–692. doi:10.1111/j.1365-313X.2005.02568.x

    Article  CAS  Google Scholar 

  • Bondada BR, Syvertsen JP (2003) Leaf chlorophyll, net gas exchange and chloroplast ultrastructure in citrus leaves of different nitrogen status. Tree Physiol 23(8):553–559

    Article  PubMed  CAS  Google Scholar 

  • Bondada BR, Syvertsen JP (2005) Concurrent changes in net CO2 assimilation and chloroplast ultrastructure in nitrogen deficient citrus leaves. Environ Exp Bot 54(1):41–48

    Article  CAS  Google Scholar 

  • Briantais J-M, Vernotte C, Picaud M, Krause G (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochimica et Biophysica Acta Bioenerg 548(1):128–138

    Article  CAS  Google Scholar 

  • Chiang YH, Zubo YO, Tapken W, Kim HJ, Lavanway AM, Howard L, Pilon M, Kieber JJ, Schaller GE (2012) Functional characterization of the GATA transcription factors GNC and CGA1 reveals their key role in chloroplast development, growth, and division in Arabidopsis. Plant Physiol 160(1):332–348. doi:10.1104/pp.112.198705

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Crosthwaite SK, Dunlap JC, Loros JJ (1997) Neurospora wc-1 and wc-2: transcription, photoresponses, and the origins of circadian rhythmicity. Science 276(5313):763–769

    Article  PubMed  CAS  Google Scholar 

  • Delvalle D, Dumez S, Wattebled F, Roldan I, Planchot V, Berbezy P, Colonna P, Vyas D, Chatterjee M, Ball S, Merida A, D’Hulst C (2005) Soluble starch synthase I: a major determinant for the synthesis of amylopectin in Arabidopsis thaliana leaves. Plant J Cell Mol Biol 43(3):398–412. doi:10.1111/j.1365-313X.2005.02462.x

    Article  CAS  Google Scholar 

  • Evans JR (1987) The dependence of quantum yield on wavelength and growth irradiance. Funct Plant Biol 14(1):69–79

    Google Scholar 

  • Evans JR (1989) Photosynthesis and nitrogen relationships in leaves of Ca plants. Oecologia 1:9–19

    Article  Google Scholar 

  • Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90

    Article  PubMed  CAS  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320(5878):889–892

    Article  PubMed  CAS  Google Scholar 

  • Gao Y, Liu H, An C, Shi Y, Liu X, Yuan W, Zhang B, Yang J, Yu C, Gao H (2013) Arabidopsis FRS4/CPD25 and FHY3/CPD45 work cooperatively to promote the expression of the chloroplast division gene ARC5 and chloroplast division. Plant J Cell Mol Biol 75(5):795–807. doi:10.1111/tpj.12240

    Article  CAS  Google Scholar 

  • Geiger DR, Bestman HD (1990) Self-limitation of herbicide mobility by phytotoxic action. Weed Sci 38(3):324–329

    CAS  Google Scholar 

  • Giles J (2005) Nitrogen study fertilizes fears of pollution. Nature 433(7028):791

    Article  PubMed  CAS  Google Scholar 

  • Hanashiro I, Itoh K, Kuratomi Y, Yamazaki M, Igarashi T, Matsugasako JI, Takeda Y (2008) Granule-bound starch synthase I is responsible for biosynthesis of extra-long unit chains of amylopectin in rice. Plant Cell Physiol 49(6):925–933. doi:10.1093/Pcp/Pcn066

    Article  PubMed  CAS  Google Scholar 

  • Hao S, Zhao T, Xia X, Yin W (2011) Genome-wide comparison of two poplar genotypes with different growth rates. Plant Mol Biol 76(6):575–591. doi:10.1007/s11103-011-9790-0

    Article  PubMed  CAS  Google Scholar 

  • Hikosaka K, Terashima I (1995) A model of the acclimation of photosynthesis in the leaves of C3 plants to sun and shade with respect to nitrogen use. Plant Cell Environ 18(6):605–618

    Article  CAS  Google Scholar 

  • Hong Y, Devaiah SP, Bahn SC, Thamasandra BN, Li M, Welti R, Wang X (2009) Phospholipase D epsilon and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. Plant J Cell Mol Biol 58(3):376–387. doi:10.1111/j.1365-313X.2009.03788.x

    Article  CAS  Google Scholar 

  • Horiguchi G, Ferjani A, Fujikura U, Tsukaya H (2006) Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana. J Plant Res 119(1):37–42. doi:10.1007/s10265-005-0232-4

    Article  PubMed  Google Scholar 

  • Hudson D, Guevara D, Yaish MW, Hannam C, Long N, Clarke JD, Bi YM, Rothstein SJ (2011) GNC and CGA1 modulate chlorophyll biosynthesis and glutamate synthase (GLU1/Fd-GOGAT) expression in Arabidopsis. PLoS ONE 6(11):e26765. doi:10.1371/journal.pone.0026765

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hudson D, Guevara DR, Hand AJ, Xu Z, Hao L, Chen X, Zhu T, Bi YM, Rothstein SJ (2013) Rice cytokinin GATA transcription factor1 regulates chloroplast development and plant architecture. Plant Physiol 162(1):132–144. doi:10.1104/pp.113.217265

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jeong MJ, Shih MC (2003) Interaction of a GATA factor with cis-acting elements involved in light regulation of nuclear genes encoding chloroplast glyceraldehyde-3-phosphate dehydrogenase in Arabidopsis. Biochem Biophys Res Commun 300(2):555–562. doi:10.1016/s0006-291x(02)02892-9

    Article  PubMed  CAS  Google Scholar 

  • Kiba T, Naitou T, Koizumi N, Yamashino T, Sakakibara H, Mizuno T (2005) Combinatorial microarray analysis revealing Arabidopsis genes implicated in cytokinin responses through the His → Asp phosphorelay circuitry. Plant Cell Physiol 46(2):339–355

    Article  PubMed  CAS  Google Scholar 

  • Kitajima K, Hogan K (2003) Increases of chlorophyll a/b ratios during acclimation of tropical woody seedlings to nitrogen limitation and high light. Plant Cell Environ 26(6):857–865

    Article  PubMed  Google Scholar 

  • Kobayashi K, Sasaki D, Noguchi K, Fujinuma D, Komatsu H, Kobayashi M, Sato M, Toyooka K, Sugimoto K, Niyogi KK, Wada H, Masuda T (2013) Photosynthesis of root chloroplasts developed in Arabidopsis lines overexpressing GOLDEN2-LIKE transcription factors. Plant Cell Physiol 54(8):1365–1377. doi:10.1093/pcp/pct086

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Krause G, Vernotte C, Briantais J-M (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae. Resolution into two components. Biochimica et Biophysica Acta Bioenerg 679(1):116–124

    Article  CAS  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu PP, Koizuka N, Martin RC, Nonogaki H (2005) The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J Cell Mol Biol 44(6):960–971. doi:10.1111/j.1365-313X.2005.02588.x

    Article  CAS  Google Scholar 

  • Luo XM, Lin WH, Zhu S, Zhu JY, Sun Y, Fan XY, Cheng M, Hao Y, Oh E, Tian M, Liu L, Zhang M, Xie Q, Chong K, Wang ZY (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19(6):872–883. doi:10.1016/j.devcel.2010.10.023

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lyu JI, Min SR, Lee JH, Lim YH, Kim J-K, Bae C-H, Liu JR (2012) Overexpression of a trehalose-6-phosphate synthase/phosphatase fusion gene enhances tolerance and photosynthesis during drought and salt stress without growth aberrations in tomato. Plant Cell Tissue Organ Cult 112(2):257–262. doi:10.1007/s11240-012-0225-7

    Article  Google Scholar 

  • MacCabe AP, Vanhanen S, Sollewijn Gelpke MD, van de Vondervoort PJ, Arst HN Jr, Visser J (1998) Identification, cloning and sequence of the Aspergillus niger areA wide domain regulatory gene controlling nitrogen utilisation. Biochimica et Biophysica Acta Gene Struct Expr 1396(2):163–168

    Article  CAS  Google Scholar 

  • Manfield IW, Devlin PF, Jen CH, Westhead DR, Gilmartin PM (2007) Conservation, convergence, and divergence of light-responsive, circadian-regulated, and tissue-specific expression patterns during evolution of the Arabidopsis GATA gene family. Plant Physiol 143(2):941–958. doi:10.1104/pp.106.090761

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mara CD, Irish VF (2008) Two GATA transcription factors are downstream effectors of floral homeotic gene action in Arabidopsis. Plant Physiol 147(2):707–718. doi:10.1104/pp.107.115634

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Marschner M (1995) Mineral nutrition of higher plants, Ed 2. Academic Press Limited, London

    Google Scholar 

  • Martinez-Carrasco R, Sanchez-Rodriguez J, Perez P (2002) Changes in chlorophyll fluorescence during the course of photoperiod and in response to drought in Casuarina equisetifolia Forst. and Forst. Photosynthetica 40(3):363–368

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51(345):659–668

    Article  PubMed  CAS  Google Scholar 

  • Naito T, Kiba T, Koizumi N, Yamashino T, Mizuno T (2007) Characterization of a unique GATA family gene that responds to both light and cytokinin in Arabidopsis thaliana. Biosci Biotechnol Biochem 71(6):1557–1560. doi:10.1271/Bbb.60692

    Article  PubMed  CAS  Google Scholar 

  • Nosengo N (2003) Fertilized to death. Nature 425(6961):894–895. doi:10.1038/425894a

    Article  PubMed  CAS  Google Scholar 

  • Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3(6):973–996. doi:10.1093/mp/ssq049

    Article  PubMed  CAS  Google Scholar 

  • Ögren E, Evans J (1993) Photosynthetic light-response curves. Planta 189(2):182–190

    Article  Google Scholar 

  • Patient RK, McGhee JD (2002) The GATA family (vertebrates and invertebrates). Curr Opin Genet Dev 12(4):416–422

    Article  PubMed  CAS  Google Scholar 

  • Ragel P, Streb S, Feil R, Sahrawy M, Annunziata MG, Lunn JE, Zeeman S, Merida A (2013) Loss of starch granule initiation has a deleterious effect on the growth of arabidopsis plants due to an accumulation of ADP-glucose. Plant Physiol 163(1):75–85. doi:10.1104/pp.113.223420

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reyes JC, Muro-Pastor MI, Florencio FJ (2004) The GATA family of transcription factors in Arabidopsis and rice. Plant Physiol 134(4):1718–1732. doi:10.1104/pp.103.037788

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Richter R, Behringer C, Muller IK, Schwechheimer C (2010) The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and phytochrome-interacting factors. Genes Dev 24(18):2093–2104. doi:10.1101/gad.594910

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ridge C, Hinckley T, Stettler R, Van Volkenburgh E (1986) Leaf growth characteristics of fast-growing poplar hybrids Populus trichocarpa× P. deltoides. Tree Physiol 1(2):209–216

    Article  PubMed  Google Scholar 

  • Sanz-Sáez Á, Erice G, Aranjuelo I, Nogués S, Irigoyen JJ, Sánchez-Díaz M (2010) Photosynthetic down-regulation under elevated CO2 exposure can be prevented by nitrogen supply in nodulated alfalfa. J Plant Physiol 167(18):1558–1565

    Article  PubMed  Google Scholar 

  • Scazzocchio C (2000) The fungal GATA factors. Curr Opin Microbiol 3(2):126–131

    Article  PubMed  CAS  Google Scholar 

  • Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136(1):2483–2499. doi:10.1104/pp.104.047019

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shangguan Z, Shao M, Dyckmans J (2000) Effects of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat. J Plant Physiol 156(1):46–51. doi:10.1016/s0176-1617(00)80271-0

    Article  CAS  Google Scholar 

  • Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30(9):1126–1149. doi:10.1111/j.1365-3040.2007.01708.x

    Article  PubMed  CAS  Google Scholar 

  • Stanbrough M, Rowen DW, Magasanik B (1995) Role of the GATA factors Gln3p and Nil1p of Saccharomyces cerevisiae in the expression of nitrogen-regulated genes. Proceedings of the National Academy of Sciences

  • Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Curr Opin Plant Biol 15(3):282–292. doi:10.1016/j.pbi.2012.03.016

    Article  PubMed  CAS  Google Scholar 

  • Taiz L, Zeiger E (2002) Plant physiology. Sinauer, EE UU California

    Google Scholar 

  • Teakle GR, Gilmartin PM (1998) Two forms of type IV zinc-finger motif and their kingdom-specific distribution between the flora, fauna and fungi. Trends Biochem Sci 23(3):100–102

    Article  PubMed  CAS  Google Scholar 

  • Teakle GR, Manfield IW, Graham JF, Gilmartin PM (2002) Arabidopsis thaliana GATA factors: organisation, expression and DNA-binding characteristics. Plant Mol Biol 50(1):43–57

    Article  PubMed  CAS  Google Scholar 

  • Tschaplinski T, Blake T (1989) Water relations, photosynthetic capacity, and root/shoot partitioning of photosynthate as determinants of productivity in hybrid poplar. Can J Bot 67(6):1689–1697

    Article  Google Scholar 

  • Verhoeven AS, Demmig-Adams B, Adams IW (1997) Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to high light and N stress. Plant Physiol 113(3):817–824

    PubMed  CAS  PubMed Central  Google Scholar 

  • von Caemmerer S (2000) Biochemical models of leaf photosynthesis, 165 PP. CSIRO Publishing, Canberra, Australia

  • Wang R, Okamoto M, Xing X, Crawford NM (2003) Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1,000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol 132(2):556–567. doi:10.1104/pp.103.021253

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Waters MT, Langdale JA (2009) The making of a chloroplast. EMBO J 28(19):2861–2873. doi:10.1038/emboj.2009.264

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yamori W, Takahashi S, Makino A, Price GD, Badger MR, von Caemmerer S (2011) The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol 155(2):956–962. doi:10.1104/pp.110.168435

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Yu F, Park S, Rodermel SR (2004) The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. Plant J Cell Mol Biol 37(6):864–876

    Article  CAS  Google Scholar 

  • Zeeman SC, Kossmann J, Smith AM (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu Rev Plant Biol 61:209–234. doi:10.1146/annurev-arplant-042809-112301

    Article  PubMed  CAS  Google Scholar 

  • Zhao D, Reddy KR, Kakani VG, Reddy V (2005) Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorghum. Eur J Agron 22(4):391–403

    Article  CAS  Google Scholar 

  • Zheng D, Han X, An Y, Guo H, Xia X, Yin W (2013) The nitrate transporter NRT2.1 functions in the ethylene response to nitrate deficiency in Arabidopsis. Plant Cell 36:1328. doi:10.1111/pce.12062

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Hi-Tech Research and Development Program of China (2013AA102701), the National Natural Science Foundation of China (31270656), 111 Project of Beijing Forestry University (B13007), Programs for Scientific Research and Graduate Training from BMEC (Regulation of Tree WUE) and Program for Changjiang Scholars and Innovative Research Team in University (IRT13047). We thank Dongchao Zheng, Dun Zhang, Congpeng Wang, and Fuling Lv for their technical assistance and helpful discussions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xinli Xia.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

An, Y., Han, X., Tang, S. et al. Poplar GATA transcription factor PdGNC is capable of regulating chloroplast ultrastructure, photosynthesis, and vegetative growth in Arabidopsis under varying nitrogen levels. Plant Cell Tiss Organ Cult 119, 313–327 (2014). https://doi.org/10.1007/s11240-014-0536-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-014-0536-y

Keywords

Navigation