Growth regulating factors (GRFs) are a conserved class of transcription factor in seed plants. GRFs are involved in various aspects of tissue differentiation and organ development. The implication of GRFs in biotic stress response has also been recently reported, suggesting a role of these transcription factors in coordinating the interaction between developmental processes and defense dynamics. However, the molecular mechanisms by which GRFs mediate the overlaps between defense signaling and developmental pathways are elusive. Here, we report large scale identification of putative target candidates of Arabidopsis GRF1 and GRF3 by comparing mRNA profiles of the grf1/grf2/grf3 triple mutant and those of the transgenic plants overexpressing miR396-resistant version of GRF1 or GRF3. We identified 1,098 and 600 genes as putative targets of GRF1 and GRF3, respectively. Functional classification of the potential target candidates revealed that GRF1 and GRF3 contribute to the regulation of various biological processes associated with defense response and disease resistance. GRF1 and GRF3 participate specifically in the regulation of defense-related transcription factors, cell-wall modifications, cytokinin biosynthesis and signaling, and secondary metabolites accumulation. GRF1 and GRF3 seem to fine-tune the crosstalk between miRNA signaling networks by regulating the expression of several miRNA target genes. In addition, our data suggest that GRF1 and GRF3 may function as negative regulators of gene expression through their association with other transcription factors. Collectively, our data provide new insights into how GRF1 and GRF3 might coordinate the interactions between defense signaling and plant growth and developmental pathways.
References
[1]
Heidel AJ, Clarke JD, Antonovics J, Dong X (2004) Fitness costs of mutations affecting the systemic acquired resistance pathway in Arabidopsis thaliana. Genetics 168: 2197–2206. doi: 10.1534/genetics.104.032193
[2]
van der Knaap E, Kim JH, Kende H (2000) A novel gibberellin-induced gene from rice and its potential regulatory role in stem growth. Plant Physiol 122: 695–704. doi: 10.1104/pp.122.3.695
[3]
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. doi: 10.1046/j.1365-313x.2003.01862.x
[4]
Choi D, Kim JH, Kende H (2004) Whole genome analysis of the OsGRF gene family encoding plant-specific putative transcription activators in rice (Oryza sativa L.). Plant Cell Physiol 45: 897–904. doi: 10.1093/pcp/pch098
[5]
Zhang DF, Li B, Jia GQ, Zhang TF, Dai JR, et al. (2008) Isolation and characterization of genes encoding GRF transcription factors and GIF transcriptional coactivators in Maize (Zea mays L.). Plant Sci 175: 809–817. doi: 10.1016/j.plantsci.2008.08.002
[6]
Kim JH, Kende H (2004) A transcriptional coactivator, AtGIF1, is involved in regulating leaf growth and morphology in Arabidopsis. Proc Natl Acad Sci U S A 101: 13374–13379. doi: 10.1073/pnas.0405450101
[7]
Kim JS, Mizoi J, Kidokoro S, Maruyama K, Nakajima J, et al. (2012) Arabidopsis growth-regulating factor7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell 24: 3393–3405. doi: 10.1105/tpc.112.100933
[8]
Liu D, Song Y, Chen Z, Yu D (2009) Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiol Plant 136: 223–236. doi: 10.1111/j.1399-3054.2009.01229.x
[9]
Rodriguez RE, Mecchia MA, Debernardi JM, Schommer C, Weigel D, et al. (2010) Control of cell proliferation in Arabidopsis thaliana by microRNA miR396. Development 137: 103–112. doi: 10.1242/dev.043067
[10]
Wang L, Gu X, Xu D, Wang W, Wang H, et al. (2011) miR396-targeted AtGRF transcription factors are required for coordination of cell division and differentiation during leaf development in Arabidopsis. J Eep Bot 62: 761–773. doi: 10.1093/jxb/erq307
[11]
Hewezi T, Baum TJ (2012) Complex feedback regulations govern the expression of miRNA396 and its GRF target genes. Plant Signal Behav 7: 749–751. doi: 10.4161/psb.20420
[12]
Casadevall R, Rodriguez RE, Debernardi JM, Palatnik JF, Casati P (2013) Repression of Growth Regulating Factors by the MicroRNA396 Inhibits Cell Proliferation by UV-B Radiation in Arabidopsis Leaves. Plant Cell 25: 3570–3583. doi: 10.1105/tpc.113.117473
[13]
Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836–843. doi: 10.1261/rna.895308
[14]
Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, et al. (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PloS One 2: e219. doi: 10.1371/journal.pone.0000219
[15]
Li Y, Zhang Q, Zhang J, Wu L, Qi Y, et al. (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiol 152: 2222–2231. doi: 10.1104/pp.109.151803
[16]
Hewezi T, Maier TR, Nettleton D, Baum TJ (2012) The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol 159: 321–335. doi: 10.1104/pp.112.193649
[17]
Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat genet 37: 501–506. doi: 10.1038/ng1543
[18]
Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, et al. (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PloS One 2: e718. doi: 10.1371/journal.pone.0000718
[19]
Chang WC, Lee TY, Huang HD, Huang HY, Pan RL (2008) PlantPAN: Plant promoter analysis navigator, for identifying combinatorial cis-regulatory elements with distance constraint in plant gene groups. BMC genomics 9: 561. doi: 10.1186/1471-2164-9-561
[20]
Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y, et al. (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci U S A 101: 8821–8826. doi: 10.1073/pnas.0402887101
[21]
Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, et al. (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18: 3073–3087. doi: 10.1105/tpc.106.045674
[22]
To JPC, Haberer G, Ferreira FJ, Deruere J, Mason MG, et al. (2004) Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell 16: 658–671. doi: 10.1105/tpc.018978
[23]
Mason MG, Mathews DE, Argyros DA, Maxwell BB, Kieber JJ, et al. (2005) Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell 17: 3007–3018. doi: 10.1105/tpc.105.035451
[24]
Verwoerd TC, Dekker BMM, Hoekema A (1989) A Small-Scale Procedure for the Rapid Isolation of Plant Rnas. Nucleic Acids Res 17: 2362–2362. doi: 10.1093/nar/17.6.2362
[25]
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262
[26]
Geer LY, Marchler-Bauer A, Geer RC, Han L, He J, et al. (2010) The NCBI BioSystems database. Nucleic Acids Res 38: D492–496. doi: 10.1093/nar/gkp858
[27]
Gutierrez L, Bussell JD, Pacurar DI, Schwambach J, Pacurar M, et al. (2009) Phenotypic Plasticity of Adventitious Rooting in Arabidopsis Is Controlled by Complex Regulation of AUXIN RESPONSE FACTOR Transcripts and MicroRNA Abundance. Plant Cell 21: 3119–3132. doi: 10.1105/tpc.108.064758
[28]
Wu G, Park MY, Conway SR, Wang JW, Weigel D, et al. (2009) The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis. Cell 138: 750–759. doi: 10.1016/j.cell.2009.06.031
[29]
Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, et al. (2010) miR390, Arabidopsis TAS3 tasiRNAs, and Their AUXIN RESPONSE FACTOR Targets Define an Autoregulatory Network Quantitatively Regulating Lateral Root Growth. Plant Cell 22: 1104–1117. doi: 10.1105/tpc.109.072553
[30]
Wang JW, Czech B, Weigel D (2009) miR156-Regulated SPL Transcription Factors Define an Endogenous Flowering Pathway in Arabidopsis thaliana. Cell 138: 738–749. doi: 10.1016/j.cell.2009.06.014
[31]
Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, et al. (2010) Orchestration of the Floral Transition and Floral Development in Arabidopsis by the Bifunctional Transcription Factor APETALA2. Plant Cell 22: 2156–2170. doi: 10.1105/tpc.110.075606
[32]
Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, et al. (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57: 771–784. doi: 10.1111/j.1365-313x.2008.03727.x
[33]
Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, et al. (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61: 698–712. doi: 10.1111/j.1365-313x.2009.04098.x
[34]
Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang YH, et al. (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol 162: 272–294. doi: 10.1104/pp.113.217026
[35]
Hwang I, Sheen J, Muller B (2012) Cytokinin Signaling Networks. Annu Rev Plant Biol 63: 353–380. doi: 10.1146/annurev-arplant-042811-105503
[36]
Ioio RD, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, et al. (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17: 678–682. doi: 10.1016/j.cub.2007.02.047
[37]
Kesarwani M, Yoo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144: 336–346. doi: 10.1104/pp.106.095299
[38]
Wang L, Fobert PR (2013) Arabidopsis clade I TGA factors regulate apoplastic defences against the bacterial pathogen Pseudomonas syringae through endoplasmic reticulum-based processes. PloS One 8: e77378. doi: 10.1371/journal.pone.0077378
[39]
Shearer HL, Cheng YT, Wang L, Liu J, Boyle P, et al. (2012) Arabidopsis clade I TGA transcription factors regulate plant defenses in an NPR1-independent fashion. Mol Plant Microbe Interact 25: 1459–1468. doi: 10.1094/mpmi-09-11-0256
[40]
Zhou J, Lee C, Zhong R, Ye ZH (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21: 248–266. doi: 10.1105/tpc.108.063321
[41]
Zhong R, Ye ZH (2012) MYB46 and MYB83 bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53: 368–380. doi: 10.1093/pcp/pcr185
[42]
O'Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, et al. (1996) Ethylene as a Signal Mediating the Wound Response of Tomato Plants. Science 274: 1914–1917. doi: 10.1126/science.274.5294.1914
[43]
Ecker JR (1995) The ethylene signal transduction pathway in plants. Science 268: 667–675. doi: 10.1126/science.7732375
[44]
Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, et al. (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8: 2309–2323. doi: 10.2307/3870470
[45]
Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, et al. (2007) Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19: 3549–3562. doi: 10.1105/tpc.107.054536
[46]
Pu L, Li Q, Fan X, Yang W, Xue Y (2008) The R2R3 MYB transcription factor GhMYB109 is required for cotton fiber development. Genetics 180: 811–820. doi: 10.1534/genetics.108.093070
[47]
Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, et al. (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21: 1453–1472. doi: 10.1105/tpc.108.062935
[48]
Raffaele S, Vailleau F, Leger A, Joubes J, Miersch O, et al. (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20: 752–767. doi: 10.1105/tpc.107.054858
[49]
Oh E, Kang H, Yamaguchi S, Park J, Lee D, et al. (2009) Genome-Wide Analysis of Genes Targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during Seed Germination in Arabidopsis. Plant Cell 21: 403–419. doi: 10.1105/tpc.108.064691
[50]
Morimoto RI (1992) Transcription factors: positive and negative regulators of cell growth and disease. Curr Opin Cell Biol 4: 480–487. doi: 10.1016/0955-0674(92)90015-5
[51]
Kesarwani M, Yoo JM, Dong XN (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144: 336–346. doi: 10.1104/pp.106.095299
[52]
Lindermayr C, Sell S, Muller B, Leister D, Durnera J (2010) Redox Regulation of the NPR1-TGA1 System of Arabidopsis thaliana by Nitric Oxide. Plant Cell 22: 2894–2907. doi: 10.1105/tpc.109.066464
[53]
Zhang YL, Fan WH, Kinkema M, Li X, Dong XN (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci U S A 96: 6523–6528. doi: 10.1073/pnas.96.11.6523
[54]
Despres C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12: 279–290. doi: 10.2307/3870928
[55]
Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, et al. (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant Microbe Interact 13: 191–202. doi: 10.1094/mpmi.2000.13.2.191
[56]
Rochon A, Boyle P, Wignes T, Fobert PR, Despres C (2006) The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18: 3670–3685. doi: 10.1105/tpc.106.046953
[57]
Choi J, Huh SU, Kojima M, Sakakibara H, Paek KH, et al. (2010) The Cytokinin-Activated Transcription Factor ARR2 Promotes Plant Immunity via TGA3/NPR1-Dependent Salicylic Acid Signaling in Arabidopsis. Dev Cell 19: 284–295. doi: 10.1016/j.devcel.2010.07.011
[58]
Choi J, Hwang I (2007) Cytokinin: Perception, signal transduction, and role in plant growth and development. J Plant Biol 50: 98–108. doi: 10.1007/bf03030617
[59]
Jameson PE, Zhang H, Lewis DH (2000) Cytokinins. Extraction, separation, and analysis. Methods Mol Biol 141: 101–121. doi: 10.1385/1-59259-067-5:101
[60]
Pertry I, Vaclavikova K, Depuydt S, Galuszka P, Spichal L, et al. (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci U S A 106: 929–934. doi: 10.1073/pnas.0811683106
[61]
Choi J, Choi D, Lee S, Ryu CM, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16: 388–394. doi: 10.1016/j.tplants.2011.03.003
[62]
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140: 411–432. doi: 10.1104/pp.105.073783
[63]
Berrocal-Lobo M, Molina A, Solano R (2002) Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J 29: 23–32. doi: 10.1046/j.1365-313x.2002.01191.x
[64]
Lu X, Zhang L, Zhang FY, Jiang WM, Shen Q, et al. (2013) AaORA, a trichome-specific AP2/ERF transcription factor of Artemisia annua, is a positive regulator in the artemisinin biosynthetic pathway and in disease resistance to Botrytis cinerea. New Phytol 198: 1191–1202. doi: 10.1111/nph.12207
[65]
Mase K, Ishihama N, Mori H, Takahashi H, Kaminaka H, et al. (2013) Ethylene-Responsive AP2/ERF Transcription Factor MACD1 Participates in Phytotoxin-Triggered Programmed Cell Death. Mol Plant Microbe Interact 26: 868–879. doi: 10.1094/mpmi-10-12-0253-r
[66]
Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, et al. (2013) ETHYLENE RESPONSE FACTOR6 Acts as a Central Regulator of Leaf Growth under Water-Limiting Conditions in Arabidopsis. Plant Physiol 162: 319–332. doi: 10.1104/pp.113.216341
[67]
McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, et al. (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139: 949–959. doi: 10.1104/pp.105.068544
[68]
Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132: 1020–1032. doi: 10.1104/pp.102.017814
[69]
Libault M, Wan JR, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact 20: 900–911. doi: 10.1094/mpmi-20-8-0900
[70]
Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, et al. (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27: 2214–2221. doi: 10.1038/emboj.2008.147
[71]
Mao GH, Meng XZ, Liu YD, Zheng ZY, Chen ZX, et al. (2011) Phosphorylation of a WRKY Transcription Factor by Two Pathogen-Responsive MAPKs Drives Phytoalexin Biosynthesis in Arabidopsis. Plant Cell 23: 1639–1653. doi: 10.1105/tpc.111.084996
[72]
Hammerschmidt R (1999) PHYTOALEXINS: What have we learned after 60 years? Annu Rev Phytopathol 37: 285–306. doi: 10.1146/annurev.phyto.37.1.285
[73]
Dixon RA (2001) Natural products and plant disease resistance. Nature 411: 843–847. doi: 10.1038/35081178
[74]
Bednarek P (2012) Chemical warfare or modulators of defence responses - the function of secondary metabolites in plant immunity. Curr Opin Plant Biol 15: 407–414. doi: 10.1016/j.pbi.2012.03.002
[75]
Hipskind JD, Paiva NL (2000) Constitutive accumulation of a resveratrol-glucoside in transgenic alfalfa increases resistance to Phoma medicaginis. Mol Plant Microbe Interact 13: 551–562. doi: 10.1094/mpmi.2000.13.5.551
[76]
Nicholson RL, Hammerschmidt R (1992) Phenolic-Compounds and Their Role in Disease Resistance. Annu Rev Phytopathol 30: 369–389. doi: 10.1146/annurev.py.30.090192.002101
Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72: 1–20. doi: 10.1016/j.plaphy.2013.05.009
[79]
Szucs I, Escobar M, Grodzinski B (2011) Emerging Roles for Plant Terpenoids. In: Moo-Young M, editor. Comprehensive biotechnology second edition: Agriculture and related biotechnologies. pp. 273–286.
[80]
Zhu QH, Helliwell CA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62: 487–495. doi: 10.1093/jxb/erq295
[81]
Mathieu J, Yant LJ, Murdter F, Kuttner F, Schmid M (2009) Repression of Flowering by the miR172 Target SMZ. Plos Biol 7: e1000148. doi: 10.1371/journal.pbio.1000148
[82]
Raman S, Greb T, Peaucelle A, Blein T, Laufs P, et al. (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55: 65–76. doi: 10.1111/j.1365-313x.2008.03483.x
[83]
Chen ZH, Bao ML, Sun YZ, Yang YJ, Xu XH, et al. (2011) Regulation of auxin response by miR393-targeted transport inhibitor response protein 1 is involved in normal development in Arabidopsis. Plant Mol Biol 77: 619–629. doi: 10.1007/s11103-011-9838-1
[84]
Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211–4218. doi: 10.1242/dev.02602
[85]
Yang FX, Liang G, Liu DM, Yu DQ (2009) Arabidopsis MiR396 Mediates the Development of Leaves and Flowers in Transgenic Tobacco. J Plant Biol 52: 475–481. doi: 10.1007/s12374-009-9061-7
[86]
Wynn AN, Rueschhoff EE, Franks RG (2011) Transcriptomic Characterization of a Synergistic Genetic Interaction during Carpel Margin Meristem Development in Arabidopsis thaliana. PloS One 6: e26231. doi: 10.1371/journal.pone.0026231
[87]
Baucher M, Moussawi J, Vandeputte OM, Monteyne D, Mol A, et al. (2013) A role for the miR396/GRF network in specification of organ type during flower development, as supported by ectopic expression of Populus trichocarpa miR396c in transgenic tobacco. Plant Biol 15: 892–898. doi: 10.1111/j.1438-8677.2012.00696.x
[88]
Liang G, He H, Li Y, Wang F, Yu D (2013) Molecular mechanism of miR396 mediating pistil development in Arabidopsis thaliana. Plant Physiol 164: 249–258. doi: 10.1104/pp.113.225144