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MADS-Box Transcription Factor AGL21 Regulates Lateral Root Development and Responds to Multiple External and Physiological Signals

Lin-Hui Yu, Zi-Qing Miao, Guo-Feng Qi and 4 more

Molecular Plant · 2014 · CC BY-NC-ND

Abstract

Plant root system morphology is dramatically influenced by various environmental cues. The adaptation of root system architecture to environmental constraints, which mostly depends on the formation and growth of lateral roots, is an important agronomic trait. Lateral root development is regulated by the external signals coordinating closely with intrinsic signaling pathways. MADS-box transcription factors are known key regulators of the transition to flowering and flower development. However, their functions in root development are still poorly understood. Here we report that AGL21, an AGL17-clade MADS-box gene, plays a crucial role in lateral root development. AGL21 was highly expressed in root, particularly in the root central cylinder and lateral root primordia. AGL21 overexpression plants produced more and longer lateral roots while agl21 mutants showed impaired lateral root development, especially under nitrogen-deficient conditions. AGL21 was induced by many plant hormones and environmental stresses, suggesting a function of this gene in root system plasticity in response to various signals. Furthermore, AGL21 was found positively regulating auxin accumulation in lateral root primordia and lateral roots by enhancing local auxin biosynthesis, thus stimulating lateral root initiation and growth. We propose that AGL21 may be involved in various environmental and physiological signals-mediated lateral root development and growth.

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References 78

1.
Achard P. Cheng H. De Grauwe L. Decat J. Schoutteten H. Moritz T. Van Der Straeten D. Peng J. Harberd N.P. (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science. 311, 91–94.
Not in our library10.1126/science.1118642
2.
Alvarez-Buylla E.R. Liljegren S.J. Pelaz S. Gold S.E. Burgeff C. Ditta G.S. Vergara-Silva F. Yanofsky M.F. (2000a) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J. 24, 457–466.
Not in our library10.1046/j.1365-313x.2000.00891.x
3.
Alvarez-Buylla E.R. Pelaz S. Liljegren S.J. Gold S.E. Burgeff C. Ditta G.S. Ribas de Pouplana L. Martinez-Castilla L. Yanofsky M.F. (2000b) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc. Natl Acad. Sci. U S A. 97, 5328–5333.
Not in our library10.1073/pnas.97.10.5328
4.
Ariel F. Diet A. Verdenaud M. Gruber V. Frugier F. Chan R. Crespi M. (2010) Environmental regulation of lateral root emergence in Medicago truncatula requires the HD-Zip I transcription factor HB1. Plant Cell. 22, 2171–2183.
Not in our library10.1105/tpc.110.074823
5.
MADS-box gene family in rice: genome-wide identification, organization and expression profiling during reproductive development and stress · 2007
No notice
6.
Becker A. Theissen G (2003) The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol. Phylogenet. Evol. 29, 464–489.
Not in our library10.1016/s1055-7903(03)00207-0
7.
Beeckman T. Burssens S. Inze D (2001) The peri-cell-cycle in Arabidopsis. J. Exp. Bot. 52, 403–411.
Not in our library10.1093/jexbot/52.suppl_1.403
8.
Benkova E. Michniewicz M. Sauer M. Teichmann T. Seifertova D. Jurgens G. Friml J. (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 115, 591–602.
Not in our library10.1016/s0092-8674(03)00924-3
9.
Burgeff C. Liljegren S.J. Tapia-Lopez R. Yanofsky M.F. Alvarez-Buylla E.R (2002) MADS-box gene expression in lateral primordia, meristems and differentiated tissues of Arabidopsis thaliana roots. Planta. 214, 365–372.
Not in our library10.1007/s004250100637
10.
Casimiro I. Marchant A. Bhalerao R.P. Beeckman T. Dhooge S. Swarup R. Graham N. Inze D. Sandberg G. Casero P.J. (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell. 13, 843–852.
Not in our library10.1105/tpc.13.4.843
11.
Clough S.J. Bent A.F (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743.
Not in our library10.1046/j.1365-313x.1998.00343.x
12.
Comstock J.P (2002) Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. J. Exp. Bot. 53, 195–200.
Not in our library10.1093/jexbot/53.367.195
13.
Curtis M.D. Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469.
Not in our library10.1104/pp.103.027979
14.
de Folter S. Shchennikova A.V. Franken J. Busscher M. Baskar >R. Grossniklaus U. Angenent G.C. Immink R.G. (2006) A Bsister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis. Plant J. 47, 934–946.
Not in our library10.1111/j.1365-313x.2006.02846.x
15.
De Smet I. Vanneste S. Inze D. Beeckman T (2006a) Lateral root initiation or the birth of a new meristem. Plant Mol. Biol. 60, 871–887.
Not in our library10.1007/s11103-005-4547-2
16.
De Smet I. Zhang H. Inze D. Beeckman T (2006b) A novel role for abscisic acid emerges from underground. Trends Plant Sci. 11, 434–439.
Not in our library10.1016/j.tplants.2006.07.003
17.
Deak K.I. Malamy J (2005) Osmotic regulation of root system architecture. Plant J. 43, 17–28.
Not in our library10.1111/j.1365-313x.2005.02425.x
18.
Engineer C.B. Kranz R.G (2007) Reciprocal leaf and root expression of AtAmt1.1 and root architectural changes in response to nitrogen starvation. Plant Physiol. 143, 236–250.
Not in our library10.1104/pp.106.088500
19.
Fukaki H. Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol. Biol. 69, 437–449.
Not in our library10.1007/s11103-008-9417-2
20.
Fukaki H. Okushima Y. Tasaka M (2007) Auxin-mediated lateral root formation in higher plants. Int. Rev. Cytol. 256, 111–137.
Not in our library10.1016/s0074-7696(07)56004-3
21.
Gan Y. Filleur S. Rahman A. Gotensparre S. Forde B.G (2005) Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta. 222, 730–742.
Not in our library10.1007/s00425-005-0020-3
22.
Garay-Arroyo A. Ortiz-Moreno E. de la Paz Sanchez M. Murphy A.S. Garcia-Ponce B. Marsch-Martinez N. de Folter S. Corvera-Poire A. Jaimes-Miranda F. Pacheco-Escobedo M.A. (2013) The MADS transcription factor XAL2/AGL14 modulates auxin transport during Arabidopsis root development by regulating PIN expression. EMBO J. 32, 2884–2895.
Not in our library10.1038/emboj.2013.216
23.
Grill E. Himmelbach A (1998) ABA signal transduction. Curr. Opin. Plant Biol. 1, 412–418.
Not in our library10.1016/s1369-5266(98)80265-3
24.
Himanen K. Boucheron E. Vanneste S. de Almeida Engler J. Inze D. Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell. 14, 2339–2351.
Not in our library10.1105/tpc.004960
25.
Hodge A (2006) Plastic plants and patchy soils. J. Exp. Bot. 57, 401–411.
Not in our library10.1093/jxb/eri280
26.
Jovanovic M. Lefebvre V. Laporte P. Gonzalez‐Rizzo S. Lelandais‐Brière C. Frugier F. Hartmann C. Crespi M. (2007) How the environment regulates root architecture in dicots. Adv Botanical Res. 46, 35–74.
Not in our library
27.
Kaufmann K. Melzer R. Theissen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene. 347, 183–198.
Not in our library10.1016/j.gene.2004.12.014
28.
Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann. Bot. 112, 1655–1665.
Not in our library10.1093/aob/mct229
29.
Krouk G. Lacombe B. Bielach A. Perrine-Walker F. Malinska K. Mounier E. Hoyerova K. Tillard P. Leon S. Ljung K. (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell. 18, 927–937.
Not in our library10.1016/j.devcel.2010.05.008
30.
Kutz A. Muller A. Hennig P. Kaiser W.M. Piotrowski M. Weiler E.W (2002) A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant J. 30, 95–106.
Not in our library10.1046/j.1365-313x.2002.01271.x
31.
Lavenus J. Goh T. Roberts I. Guyomarc’h S. Lucas M. De Smet I. Fukaki H. Beeckman T. Bennett M. Laplaze L. (2013) Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 18, 450–458.
Not in our library10.1016/j.tplants.2013.04.006
32.
Lee R.D. Cho H.T (2013) Auxin, the organizer of the hormonal/environmental signals for root hair growth. Front Plant Sci. 4, 448.
Not in our library10.3389/fpls.2013.00448
33.
Lei Z.Y. Zhao P. Cao M.J. Cui R. Chen X. Xiong L.Z. Zhang Q.F. Oliver D.J. Xiang C.B. (2007) High-throughput binary vectors for plant gene function analysis. Journal of Integrative Plant Biology. 49, 556–567.
Not in our library
34.
Leyser O. Fitter A (1998) Roots are branching out in patches. Trends Plant Sci. 3, 203–204.
Not in our library
35.
Lin W.H. Wang Y. Mueller-Roeber B. Brearley C.A. Xu Z.H. Xue H.W (2005) At5PTase13 modulates cotyledon vein development through regulating auxin homeostasis. Plant Physiol. 139, 1677–1691.
Not in our library10.1104/pp.105.067140
36.
Linkohr B.I. Williamson L.C. Fitter A.H. Leyser H.M (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J. 29, 751–760.
Not in our library10.1046/j.1365-313x.2002.01251.x
37.
Lloret P.G. Casero P.J. (2002) Lateral root initiation. In Plant roots: the hidden half, 3rd ed., Waisel, Y., Eshel, A., Kafkafi, U., eds. (New York: Marcel Dekker), pp. 127–156.
Not in our library
38.
Lopez-Bucio J. Cruz-Ramirez A. Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6, 280–287.
Not in our library10.1016/s1369-5266(03)00035-9
39.
Lopez-Bucio J. Hernandez-Abreu E. Sanchez-Calderon L. Nieto-Jacobo M.F. Simpson J. Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129, 244–256.
Not in our library10.1104/pp.010934
40.
Lynch J.P (2007) Roots of the second green revolution. Aust. J. Bot. 55, 493–512.
Not in our library
41.
Malamy J.E (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28, 67–77.
Not in our library10.1111/j.1365-3040.2005.01306.x
42.
Malamy J.E. Benfey P.N (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development. 124, 33–44.
Not in our library10.1242/dev.124.1.33
43.
Malamy J.E. Ryan K.S (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol. 127, 899–909.
Not in our library
44.
Menkens A.E. Schindler U. Cashmore A.R (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIP proteins. Trends Biochem. Sci. 20, 506–510.
Not in our library10.1016/s0968-0004(00)89118-5
45.
Messenguy F. Dubois E (2003) Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene. 316, 1–21.
Not in our library10.1016/s0378-1119(03)00747-9
46.
Montiel G. Gantet P. Jay-Allemand C. Breton C (2004) Transcription factor networks: pathways to the knowledge of root development. Plant Physiol. 136, 3478–3485.
Not in our library10.1104/pp.104.051029
47.
Nakagawa T. Suzuki T. Murata S. Nakamura S. Hino T. Maeo K. Tabata R. Kawai T. Tanaka K. Niwa Y. (2007) Improved Gateway binary vectors: high-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095–2100.
Not in our library10.1271/bbb.70216
48.
Nibau C. Gibbs D.J. Coates J.C (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol. 179, 595–614.
Not in our library10.1111/j.1469-8137.2008.02472.x
49.
Osmont K.S. Sibout R. Hardtke C.S (2007) Hidden branches: developments in root system architecture. Annu. Rev. Plant Biol. 58, 93–113.
Not in our library10.1146/annurev.arplant.58.032806.104006
50.
Parenicova L. de Folter S. Kieffer M. Horner D.S. Favalli C. Busscher J. Cook H.E. Ingram R.M. Kater M.M. Davies B. (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell. 15, 1538–1551.
Not in our library10.1105/tpc.011544
51.
Peret B. De Rybel B. Casimiro I. Benkova E. Swarup R. Laplaze L. Beeckman T. Bennett M.J. (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci. 14, 399–408.
Not in our library10.1016/j.tplants.2009.05.002
52.
Pinyopich A. Ditta G.S. Savidge B. Liljegren S.J. Baumann E. Wisman E. Yanofsky M.F. (2003) Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature. 424, 85–88.
Not in our library10.1038/nature01741
53.
Puig J. Meynard D. Khong G.N. Pauluzzi G. Guiderdoni E. Gantet P (2013) Analysis of the expression of the AGL17-like clade of MADS-box transcription factors in rice. Gene Expr. Patterns. 13, 160–170.
Not in our library10.1016/j.gep.2013.02.004
54.
Raya-Gonzalez J. Pelagio-Flores R. Lopez-Bucio J (2012) The jasmonate receptor COI1 plays a role in jasmonate-induced lateral root formation and lateral root positioning in Arabidopsis thaliana. J. Plant Physiol. 169, 1348–1358.
Not in our library10.1016/j.jplph.2012.05.002
55.
Reed R.C. Brady S.R. Muday G.K (1998) Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiol. 118, 1369–1378.
Not in our library10.1104/pp.118.4.1369
56.
Ripoll J.J. Roeder A.H. Ditta G.S. Yanofsky M.F (2011) A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development. 138, 5167–5176.
Not in our library10.1242/dev.073031
57.
Saedler H. Becker A. Winter K.U. Kirchner C. Theissen G (2001) MADS-box genes are involved in floral development and evolution. Acta Biochim. Pol. 48, 351–358.
Not in our library
58.
Samach A. Onouchi H. Gold S.E. Ditta G.S. Schwarz-Sommer Z. Yanofsky M.F. Coupland G. (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science. 288, 1613–1616.
Not in our library10.1126/science.288.5471.1613
59.
Seki M. Narusaka M. Ishida J. Nanjo T. Fujita M. Oono Y. Kamiya A. Nakajima M. Enju A. Sakurai T. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279–292.
Not in our library10.1046/j.1365-313x.2002.01359.x
60.
Serraj R. Kumar A. McNally K.L. Slamet-Loedin I. Bruskiewich R. Mauleon R. Cairns J. Hijmans R.J. (2009) Improvement of drought resistance in rice. Adv. Agron. 103, 41–99.
Not in our library
61.
Sessa G. Meller Y. Fluhr R (1995) A GCC element and a G-box motif participate in ethylene-induced expression of the PRB-1b gene. Plant Mol. Biol. 28, 145–153.
Not in our library10.1007/bf00042046
62.
Stals H. Inze D (2001) When plant cells decide to divide. Trends Plant Sci. 6, 359–364.
Not in our library10.1016/s1360-1385(01)02016-7
63.
Sun J. Xu Y. Ye S. Jiang H. Chen Q. Liu F. Zhou W. Chen R. Li X. Tietz O. (2009) Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell. 21, 1495–1511.
Not in our library10.1105/tpc.108.064303
64.
Suzuki A. Miyamoto M. Forde Brian G. Takahashi H (2009) Nitrogen-regulated transcription factor, AGL21, controls lateral root development in Arabidopsis [abstract]. 20th International Conference on Arabidopsis Research, Edinburgh, UK.
Not in our library
65.
Svistoonoff S. Creff A. Reymond M. Sigoillot-Claude C. Ricaud L. Blanchet A. Nussaume L. Desnos T. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39, 792–796.
Not in our library10.1038/ng2041
66.
Tapia-Lopez R. Garcia-Ponce B. Dubrovsky J.G. Garay-Arroyo A. Perez-Ruiz R.V. Kim S.H. Acevedo F. Pelaz S. Alvarez-Buylla E.R. (2008) An AGAMOUS-related MADS-box gene, XAL1 (AGL12), regulates root meristem cell proliferation and flowering transition in Arabidopsis. Plant Physiol. 146, 1182–1192.
Not in our library10.1104/pp.107.108647
67.
Teale W.D. Ditengou F.A. Dovzhenko A.D. Li X. Molendijk A.M. Ruperti B. Paponov I. Palme K. (2008) Auxin as a model for the integration of hormonal signal processing and transduction. Mol. Plant. 1, 229–237.
Not in our library10.1093/mp/ssn006
68.
Ticconi C.A. Delatorre C.A. Lahner B. Salt D.E. Abel S (2004) Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J. 37, 801–814.
Not in our library10.1111/j.1365-313x.2004.02005.x
69.
Ulmasov T. Hagen G. Guilfoyle T.J (1999) Dimerization and DNA binding of auxin response factors. Plant J. 19, 309–319.
Not in our library10.1046/j.1365-313x.1999.00538.x
70.
Ulmasov T. Murfett J. Hagen G. Guilfoyle T.J (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 9, 1963–1971.
Not in our library10.1105/tpc.9.11.1963
71.
Vidal E.A. Araus V. Lu C. Parry G. Green P.J. Coruzzi G.M. Gutierrez R.A. (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 107, 4477–4482.
Not in our library10.1073/pnas.0909571107
72.
Wolters H. Jurgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat. Rev. Genet. 10, 305–317.
Not in our library10.1038/nrg2558
73.
Woodward A.W. Bartel B (2005) Auxin: regulation, action, and interaction. Ann. Bot. 95, 707–735.
Not in our library10.1093/aob/mci083
74.
Wu Y. Zhao Q. Gao L. Yu X.M. Fang P. Oliver D.J. Xiang C.B. (2010) Isolation and characterization of low-sulphur-tolerant mutants of Arabidopsis. J. Exp. Bot. 61, 3407–3422.
Not in our library10.1093/jxb/erq161
75.
Xi J. Xu P. Xiang C.B (2012) Loss of AtPDR11, a plasma membrane-localized ABC transporter, confers paraquat tolerance in Arabidopsis thaliana. Plant J. 69, 782–791.
Not in our library10.1111/j.1365-313x.2011.04830.x
76.
Xu B. Timko M (2004) Methyl jasmonate induced expression of the tobacco putrescine N-methyltransferase genes requires both G-box and GCC-motif elements. Plant Mol. Biol. 55, 743–761.
Not in our library10.1007/s11103-004-1962-8
77.
Yu L. Chen X. Wang Z. Wang S. Wang Y. Zhu Q. Li S. Xiang C. (2013) Arabidopsis Enhanced Drought Tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield penalty. Plant Physiol. 162, 1378–1391.
Not in our library10.1104/pp.113.217596
78.
Zhang H. Forde B.G (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science. 279, 407–409.
Not in our library10.1126/science.279.5349.407

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