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The role of GRAS proteins in plant signal transduction and development

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Abstract

GRAS proteins are a recently discovered family of plant-specific proteins named after GAI, RGA and SCR, the first three of its members isolated. Although the Arabidopsis genome encodes at least 33 GRAS protein family members only a few GRAS proteins have been characterized so far. However, it is becoming clear that GRAS proteins exert important roles in very diverse processes such as signal transduction, meristem maintenance and development. Here we present a survey of the different GRAS proteins and review the current knowledge of the function of individual members of this protein family.

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References

  • Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–180

    CAS  PubMed  Google Scholar 

  • Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14:1269–1278

    CAS  PubMed  Google Scholar 

  • Boutet S, Vazquez F, Liu J, Beclin C, Fagard M, Gratias A, Morel JB, Crete P, Chen X, Vaucheret H (2003) Arabidopsis HEN1. A genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr Biol 13:843–848

    Article  CAS  PubMed  Google Scholar 

  • Carles CC, Fletcher JC (2003) Shoot apical meristem maintenance: the art of a dynamic balance. Trends Plant Sci 8:394–401

    Article  CAS  PubMed  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

    Article  CAS  PubMed  Google Scholar 

  • Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129:181–190

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Liu J, Cheng Y, Jia D (2002) HEN1 functions pleiotropically in Arabidopsis development and acts in C function in the flower. Development 129:1085–1094

    Article  CAS  PubMed  Google Scholar 

  • Day RB, Shibuya N, Minami E (2003) Identification and characterization of two new members of the GRAS gene family in rice responsive to N-acetylchitooligosaccharide elicitor. Biochim Biophys Acta 1625:261–268

    Article  CAS  PubMed  Google Scholar 

  • Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    PubMed  Google Scholar 

  • Dill A, Sun TP (2001) Synergistic derepression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159:777–785

    CAS  PubMed  Google Scholar 

  • Dill A, Jung HS, Sun TP (2001) The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA 98:14162–14167

    Article  CAS  PubMed  Google Scholar 

  • Eckardt NA (2002) Foolish seedlings and DELLA regulators: the functions of rice SLR1 and Arabidopsis RGL1 in GA signal transduction. Plant Cell 14:1–5

    Article  PubMed  Google Scholar 

  • Fleck B, Harberd NP (2002) Evidence that the Arabidopsis nuclear gibberellin signalling protein GAI is not destabilised by gibberellin. Plant J 32:935–947

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200

    Google Scholar 

  • Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M (1998) Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14:425–430

    Article  CAS  PubMed  Google Scholar 

  • Gerber HP, Seipel K, Georgiev O, Hofferer M, Hug M, Rusconi S, Schaffner W (1994) Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science 263:808–811

    CAS  PubMed  Google Scholar 

  • Golden TA, Schauer SE, Lang JD, Pien S, Mushegian AR, Grossniklaus U, Meinke DW, Ray A (2002) SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol 130:808–822

    PubMed  Google Scholar 

  • Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17:1175–1187

    Article  CAS  PubMed  Google Scholar 

  • Halliday K, Fankhauser C (2003) Phytochrome-hormonal signalling networks. New Phytol 157:449–459

    Article  CAS  Google Scholar 

  • Hedden P (2003) The genes of the green revolution. Trends Genet 19:5–9

    Article  CAS  PubMed  Google Scholar 

  • Heery DM, Kalkhoven E, Hoare S, Parker MG (1997) A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature 387:733–736

    CAS  PubMed  Google Scholar 

  • Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    CAS  PubMed  Google Scholar 

  • Hunter C, Poethig RS (2003) miSSING LINKS: miRNAs and plant development. Curr Opin Genet Dev 13:372–378

    Article  CAS  PubMed  Google Scholar 

  • Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010

    CAS  PubMed  Google Scholar 

  • Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70

    Google Scholar 

  • Kamiya N, Itoh JI, Morikami A, Nagato Y, Matsuoka M (2003) The SCARECROW gene’s role in asymmetric cell divisions in rice plants. Plant J 36:45–54

    Article  CAS  PubMed  Google Scholar 

  • Kidner CA, Martienssen RA (2003) Macro effects of microRNAs in plants. Trends Genet 19:13–16

    CAS  PubMed  Google Scholar 

  • Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Lo J, Harberd NP, Peng J (2002a) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Jeon K, Lee JT, Kim S, Kim VN (2002b) MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670

    CAS  PubMed  Google Scholar 

  • Lenhard M, Jurgens G, Laux T (2002) The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation. Development 129:3195–3206

    CAS  PubMed  Google Scholar 

  • Levy DE, Darnell JE Jr (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3:651–662

    Article  CAS  PubMed  Google Scholar 

  • Li X, Qian Q, Fu Z, Wang Y, Xiong G, Zeng D, Wang X, Liu X, Teng S, Hiroshi F, Yuan M, Luo D, Han B, Li J (2003) Control of tillering in rice. Nature 422:618–621

    Article  CAS  PubMed  Google Scholar 

  • Lim J, Helariutta Y, Specht CD, Jung J, Sims L, Bruce WB, Diehn S, Benfey PN (2000) Molecular analysis of the SCARECROW gene in maize reveals a common basis for radial patterning in diverse meristems. Plant Cell 12:1307–1318

    Article  CAS  PubMed  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002a) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619

    Google Scholar 

  • Llave C, Xie Z, Kasschau KD, Carrington JC (2002b) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    CAS  PubMed  Google Scholar 

  • McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM (2003) The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15:1120–1130

    Google Scholar 

  • Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629–639

    Google Scholar 

  • Morelli G, Ruberti I (2002) Light and shade in the photocontrol of Arabidopsis growth. Trends Plant Sci 7:399–404

    Article  CAS  PubMed  Google Scholar 

  • Morohashi K, Minami M, Takase H, Hotta Y, Hiratsuka K (2003) Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J Biol Chem 278:20865–20873

    Article  CAS  PubMed  Google Scholar 

  • Nakajima K, Benfey PN (2002) Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell [Suppl] 14:265–276

    Google Scholar 

  • Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311

    Article  CAS  PubMed  Google Scholar 

  • Ogawa M, Kusano T, Katsumi M, Sano H (2000) Rice gibberellin-insensitive gene homolog, OsGAI, encodes a nuclear-localized protein capable of gene activation at transcriptional level. Gene 245:21–29

    Article  CAS  PubMed  Google Scholar 

  • Olszewski N, Sun TP, Gubler F (2002) Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell [Suppl] 14:61–80

    Google Scholar 

  • Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495

    CAS  PubMed  Google Scholar 

  • Pasquinelli AE, Ruvkun G (2002) Control of developmental timing by microRNAs and their targets. Annu Rev Cell Dev Biol 18:495–513

    Article  CAS  PubMed  Google Scholar 

  • Patschinsky T, Hunter T, Esch FS, Cooper JA, Sefton BM (1982) Analysis of the sequence of amino acids surrounding sites of tyrosine phosphorylation. Proc Natl Acad Sci USA 79:973–977

    CAS  PubMed  Google Scholar 

  • Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205

    CAS  PubMed  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    CAS  PubMed  Google Scholar 

  • Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119

    Article  PubMed  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    CAS  PubMed  Google Scholar 

  • Remington DL, Purugganan MD (2002) GAI homologues in the Hawaiian silversword alliance (AsteraceaeMadiinae): molecular evolution of growth regulators in a rapidly diversifying plant lineage. Mol Biol Evol 19:1563–1574

    CAS  PubMed  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    CAS  PubMed  Google Scholar 

  • Richards DE, Peng J, Harberd NP (2000) Plant GRAS and metazoan STATs: one family? Bioessays 22:573–577

    Article  CAS  PubMed  Google Scholar 

  • Richards DE, King KE, Ait-Ali T, Harberd NP (2001) How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. Annu Rev Plant Physiol Plant Mol Biol 52:67–88

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358

    Article  CAS  PubMed  Google Scholar 

  • Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–1898

    Article  CAS  PubMed  Google Scholar 

  • Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7:487–491

    CAS  PubMed  Google Scholar 

  • Schumacher K, Schmitt T, Rossberg M, Schmitz G, Theres K (1999) The Lateral suppressor (Ls) gene of tomato encodes a new member of the VHIID protein family. Proc Natl Acad Sci USA 96:290–295

    CAS  PubMed  Google Scholar 

  • Silverstone AL, Sun T (2000) Gibberellins and the green revolution. Trends Plant Sci 5:1–2

    Article  CAS  PubMed  Google Scholar 

  • Silverstone AL, Ciampaglio CN, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169

    CAS  PubMed  Google Scholar 

  • Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, Sun TP (2001) Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13:1555–1566

    Google Scholar 

  • Stuurman J, Jaggi F, Kuhlemeier C (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16:2213–2218

    Article  CAS  PubMed  Google Scholar 

  • Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17:49–63

    CAS  PubMed  Google Scholar 

  • Vierstra RD (2003) The ubiquitin/26S proteasome pathway, the complex last chapter in the life of many plant proteins. Trends Plant Sci 8:135–142

    Article  CAS  PubMed  Google Scholar 

  • Wen CK, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100

    Google Scholar 

  • Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN (2000) Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127:595–603

    CAS  PubMed  Google Scholar 

  • Xia X, Xie Z (2001) DAMBE: Data analysis in molecular biology and evolution. J Hered 92:371–373

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

I thank Reinhold G. Herrmann, Randy Foster and the members of the group for useful discussion and critical reading of the manuscript. I am grateful to Nam-Hai Chua for support during the first stages of this project. My thanks to Philip Benfey for sharing information before publication. I apologize to those colleagues whose work was not cited because of space limitations. Work in my laboratory is supported by the Deutsche Forschungsgemeinschaft (DFG) and the Arabidopsis Functional Genomics Network (AFGN, grant no. BO 1146/4-1 to C.B.).

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Correspondence to Cordelia Bolle.

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Bolle, C. The role of GRAS proteins in plant signal transduction and development. Planta 218, 683–692 (2004). https://doi.org/10.1007/s00425-004-1203-z

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