Skip to main content

Advertisement

Log in

The BIG gene is required for auxin-mediated organ growth in Arabidopsis

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Control of organ size by cell expansion and cell proliferation is a fundamental process during development, but the importance of BIG in this process is still poorly understood. Here, we report the isolation and characterization of a new allele mutant of BIG in Arabidopsis: big-j588. The mutant displayed small aerial organs that were characterized by reduced cell size in the epidermis and short roots with decreased cell numbers. The big-j588 axr1 double and big-j588 arf7 arf19 triple mutants displayed more severe defects in leaf expansion and root elongation than their parents, implying BIG is involved in auxin-dependent organ growth. Genetic analysis suggests that BIG may act synergistically with PIN1 to affect leaf growth. The PIN1 protein level decreased in both the root cells and the tips of leaf pavement cell lobes of big-j588. Further analysis showed that the auxin maxima in the roots and the leaves of big-j588 decreased. Therefore, we concluded that the small leaves and the short roots of big-j588 were associated with reduction of auxin maxima. Overall, our study suggested that BIG is required for Arabidopsis organ growth via auxin action.

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
Fig. 7

Similar content being viewed by others

Abbreviations

IAA:

Indole-3-acetic acid

NAA:

1-Naphthaleneacetic acid

NPA:

N-1-Naphthylphthalamic acid

PI:

Propidium iodide

X-Gluc:

5-Bromo-4-chloro-3-indolyl β-d-glucuronide

References

  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  PubMed  Google Scholar 

  • Berger D, Altmann T (2000) A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev 14:1119–1131

    PubMed  CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    Article  Google Scholar 

  • Candela H, Martinez-Laborda A, Micol JL (1999) Venation pattern formation in Arabidopsis thaliana vegetative leaves. Dev Biol 205:205–216

    Article  PubMed  CAS  Google Scholar 

  • Chen JG, Shimomura S, Sitbon F, Sandberg G, Jones AM (2001) The role of auxin-binding protein 1 in the expansion of tobacco leaf cells. Plant J 28:607–617

    Article  PubMed  CAS  Google Scholar 

  • Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell 19:2430–2439

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Colon-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508

    Article  PubMed  CAS  Google Scholar 

  • Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92

    Article  PubMed  CAS  Google Scholar 

  • Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419

    Article  PubMed  CAS  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    PubMed  CAS  Google Scholar 

  • Ferjani A, Horiguchi G, Yano S, Tsukaya H (2007) Analysis of leaf development in fugu mutants of Arabidopsis reveals three compensation modes that modulate cell expansion in determinate organs. Plant Physiol 144:988–999

    Article  PubMed  CAS  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  PubMed  CAS  Google Scholar 

  • Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z (2005) Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700

    Article  PubMed  CAS  Google Scholar 

  • Fujikura U, Horiguchi G, Ponce MR, Micol JL, Tsukaya H (2009) Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana. Plant J 59:499–508

    Article  PubMed  CAS  Google Scholar 

  • Ganguly A, Lee SH, Cho M, Lee OR, Yoo H, Cho HT (2010) Differential auxin-transporting activities of PIN-FORMED proteins in Arabidopsis root hair cells. Plant Physiol 153:1046–1061

    Article  PubMed  CAS  Google Scholar 

  • Gardner MJ, Baker AJ, Assie JM, Poethig RS, Haseloff JP, Webb AA (2009) GAL4 GFP enhancer trap lines for analysis of stomatal guard cell development and gene expression. J Exp Bot 60:213–226

    Article  PubMed  CAS  Google Scholar 

  • Gil P, Dewey E, Friml J, Zhao Y, Snowden KC, Putterill J, Palme K, Estelle M, Chory J (2001) BIG: a calossin-like protein required for polar auxin transport in Arabidopsis. Genes Dev 15:1985–1997

    Article  PubMed  CAS  Google Scholar 

  • Guenot B, Bayer E, Kierzkowski D, Smith RS, Mandel T, Zadnikova P, Benkova E, Kuhlemeier C (2012) PIN1-Independent Leaf Initiation in Arabidopsis. Plant Physiol 159:1501–1510

    Article  PubMed  CAS  Google Scholar 

  • Hamada S, Onouchi H, Tanaka H, Kudo M, Liu Y-G, Shibata D, Machida C, Machida Y (2000) Mutations in the WUSCHEL gene of Arabidopsis thaliana result in the development of shoots without juvenile leaves. Plant J 24:91–101

    Article  PubMed  CAS  Google Scholar 

  • Hay A, Barkoulas M, Tsiantis M (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133:3955–3961

    Article  PubMed  CAS  Google Scholar 

  • Horiguchi G, Kim G-T, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. Plant J 43:68–78

    Article  PubMed  CAS  Google Scholar 

  • Hu Y, Xie Q, Chua NH (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961

    Article  PubMed  CAS  Google Scholar 

  • Jing Y, Cui D, Bao F, Hu Z, Qin Z, Hu Y (2009) Tryptophan deficiency affects organ growth by retarding cell expansion in Arabidopsis. Plant J 57:511–521

    Article  PubMed  CAS  Google Scholar 

  • Jones AM (1998) Auxin-Dependent Cell Expansion Mediated by Overexpressed Auxin-Binding Protein 1. Science 282:1114–1117

    Article  PubMed  CAS  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 

  • Kawade K, Horiguchi G, Tsukaya H (2010) Non-cell-autonomously coordinated organ size regulation in leaf development. Development 137:4221–4227

    Article  PubMed  CAS  Google Scholar 

  • Kim GT, Tsukaya H, Uchimiya H (1998) The ROTUNDIFOLIA3 gene of Arabidopsis thaliana encodes a new member of the cytochrome P-450 family that is required for the regulated polar elongation of leaf cells. Genes Dev 12:2381–2391

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104

    Article  PubMed  CAS  Google Scholar 

  • Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J 4:403–410

    Article  PubMed  CAS  Google Scholar 

  • Leyser O (2002) Molecular genetics of auxin signaling. Annu Rev Plant Biol 53:377–398

    Article  PubMed  CAS  Google Scholar 

  • Lincoln C, Britton JH, Estelle M (1990) Growth and development of the axr1 mutants of Arabidopsis. Plant Cell 2:1071–1080

    PubMed  CAS  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Pérez-Torres A, Rampey RA, Bartel B, Herrera-Estrella L (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691

    Article  PubMed  Google Scholar 

  • Mattsson J, Ckurshumova W, Berleth T (2003) Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol 131:1327–1339

    Article  PubMed  CAS  Google Scholar 

  • Mizukami Y (2001) A matter of size: developmental control of organ size in plants. Curr Opin Plant Biol 4:533–539

    Article  PubMed  CAS  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio agsays with tohaoco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, Fukuda H, Goodrich J, Tsukaya H (2004) Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Plant J 38:699–713

    Article  PubMed  CAS  Google Scholar 

  • Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. Plant Cell 3:677–684

    PubMed  CAS  Google Scholar 

  • Okushima Y, Mitina I, Quach HL, Theologis A (2005) AUXIN RESPONSE FACTOR 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46

    Article  PubMed  CAS  Google Scholar 

  • Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof YD, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256

    Article  PubMed  CAS  Google Scholar 

  • Perez–Perez JM, Candela H, Robles P, Lopez-Torrejon G, del Pozo JC, Micol JL (2010) A role for AUXIN RESISTANT3 in the coordination of leaf growth. Plant Cell Physiol 51:1661–1673

    Article  PubMed  Google Scholar 

  • Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harbor perspectives in biology 2:a001446

    Article  PubMed  Google Scholar 

  • Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12:507–518

    PubMed  CAS  Google Scholar 

  • Ruegger M, Dewey E, Hobbie L, Brown D, Bernasconi Turner PJ, Muday G, Estelle M (1997) Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. Plant Cell 9:745–757

    PubMed  CAS  Google Scholar 

  • Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999) An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–472

    Article  PubMed  CAS  Google Scholar 

  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133:251–261

    Article  PubMed  CAS  Google Scholar 

  • Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol 121:1179–1190

    Article  PubMed  CAS  Google Scholar 

  • Timpte CS, Wilson AK, Estelle M (1992) Effects of the axr2 mutation of Arabidopsis on cell shape in hypocotyl and inflorescence. Planta 188:271–278

    Article  CAS  Google Scholar 

  • Tsuge T, Tsukaya H, Uchimiya H (1996) Two independent and polarized processes of cell elongation regulate leaf blade expansion in Arabidopsis thaliana (L.) Heynh. Development 122:1589–1600

    PubMed  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    PubMed  CAS  Google Scholar 

  • Wilmoth JC, Wang S, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, Alonso JM, Ecker JR, Reed JW (2005) NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 43:118–130

    Article  PubMed  CAS  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi N, Suzuki M, Fukaki H, Morita-Terao M, Tasaka M, Komeda Y (2007) CRM1/BIG-mediated auxin action regulates Arabidopsis inflorescence development. Plant Cell Physiol 48:1275–1290

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to Liping Guan for confocal images, P. Doerner for the CycB1-GUS, T. Guilfoyle for DR5-GUS and J. Friml for DR5-GFP and PIN1-GFP seeds. This work was supported by the Ministry of Agriculture of the People’s Republic of China (Grant NO. 2013ZX08009-003-002, 2009ZX08009-029B), the National Natural Science Foundation of China (NSFC) (Grant NO. 31070247, 91017002, 31271460).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suiwen Hou.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 7694 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guo, X., Lu, W., Ma, Y. et al. The BIG gene is required for auxin-mediated organ growth in Arabidopsis. Planta 237, 1135–1147 (2013). https://doi.org/10.1007/s00425-012-1834-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-012-1834-4

Keywords

Navigation