Abstract
Plant development relies on the capacity of cells to interpret positional information and translate it into proliferation, elongation, and differentiation programs. ALTERED MERISTEM PROGRAM 1 (AMP1) encodes a putative glutamate carboxypeptidase involved in embryo development, plant growth, and phytohormone homeostasis. Here, we show that mutations of AMP1 cause defective seed coat formation, which correlates with increased frequency of embryo abortion, low seed production, and retarded germination. Seed alterations in amp1 mutants were related to decreased production of trichomes on leaves and increased ratio of short or bifurcated root hairs in primary roots and primary root growth inhibition. Expression analyses of hormone-related gene constructs TCS::GFP, DR5:uidA, and pABI4:uidA indicated that slow root growth is likely independent of cytokinin and auxin signaling and involves changes in abscisic acid responsiveness. Our data show that AMP1 is necessary for normal seed coat and embryo establishment during seed development and plays an important role in post-embryonic root growth and epidermal cell elongation.
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Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:1–19
Arsovski AA, Haughn GW, Western TL (2010) Seed coat mucilage cells of Arabidopsis thaliana as a model for plant cell wall research. Plant Signal Behav 5:796–801
Bäumlein H, Miséra S, Luerssen H, Kölle K, Horstmann C, Wobus U, Müller AJ (1994) The FUS3 gene of Arabidopsis thaliana is a regulator of gene expression during late embryogenesis. Plant J 6:379–387
Benfey P (1999) Is the shoot a root with a view? Curr Opin Plant Biol 2:39–43
Berger F, Grini PE, Schnittger A (2006) Endosperm: an integrator of seed growth and development. Curr Opin Plant Biol 9:664–670
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
Bleecker AB, Estelle MA, Somerville C, Kende H (1988) Insensitivity to ethylene conferred by a dominant mutation in Arabidopsis thaliana. Science 241:1086–1089
Bossi F, Cordoba E, Dupre P, Santos M, San Roman C, León P (2009) The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. Plant J 59:359–374
Brarybrook S, Stone L, Park S, Bur AQ, Lee BH Fischer RL, Goldberg RB, Harada JJ (2006) Genes directly regulated by leaf cotyledon 2 provides insight into the control of embryo maturation and somatic embryogenesis. Proc Natl Acad Sci USA 103:3468–3473
Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14:867–876
Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng X, Wang JY, Lee MM, Benfey P, Woolf PJ, Schiefelbein J (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8:e1002446
Bush SM, Krysan PJ (2007) Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in another, inflorescence, and embryo development. J Exp Bot 58:2181–2191
Casson SA, Hetherington AM (2010) Environmental regulation of stomatal development. Curr Opin Plant Biol 13:90–95
Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585
Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, Ecker J (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89:1133–1144
Chaudhury AM, Letham S, Craig S, Dennis ES (1993) AMP1 a mutant with high cytokinin levels and altered embryonic pattern, faster vegetative growth, constitutive photomorphogenesis and precocious flowering. Plant J 4:907–916
Chen LQ, Lin W, Qu XQ, Sosso D, McFarlane HE, Londoño A, Samuels L, Frommer W (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:607–619
Chin-Atkins A, Craig S, Hocart C, Dennis E, Chaudhury A (1996) Increased endogenous cytokinin in the Arabidopsis amp1 mutant corresponds with de-etiolation responses. Planta 198:549–556
Chiu RS, Nahal H, Provart NJ, Gazzarrini S (2012) The role of the Arabidopsis FUSCA3 transcription factor during inhibition of seed germination at high temperature. BMC Plant Biol 12:15
Chory J, Nagpal P, Peto CA (1991) Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3:445–459
Debeaujon I, Léon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122:403–414
Dekkers BJ, Pearce S, van Bolderen-Veldkamp RP et al (2013) Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiol 163:205–215
Figueiredo DD, Köhler C (2014) Signalling events regulating seed coat development. Biochem Soc Trans 42:358–363
Finkelstein R (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5:765–771
Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell 10:1043–1054
Focks N, Benning C (1998) wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol 118:91–101
Fukaki H, Tameda S, Masuda H, Tasaka M (2002) Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J 29:153–168
Gallavotti A (2013) The role of auxin in shaping shoot architecture. J Exp Bot 64:2593–2608
Glover B (2000) Differentiation in plant epidermal cells. J Exp Bot 51:497–505
Griffiths J, Barrero JM, Taylor J, Helliwell CA, Gubler F (2011) ALTERED MERISTEM PROGRAM 1 is involved in development of seed dormancy in Arabidopsis. PLoS One 6:e20408
Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103
Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523
Hanke DE, Northcote DH (1975) Molecular visualization of pectin and DNA by ruthenium red. Biopolymers 14:1–17
Haughn G, Chaudhury A (2005) Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci 10:472–477
Haughn G, Western T (2012) Arabidopsis seed coat mucilage is a specialized cell wall that can be used as a model for genetic analysis of plant cell wall structure and function. Front Plant Sci 3:64
Hehenberger E, Kradolfer D, Köhler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139:2031–2039
Helliwell CA, Chin-Atkins AN, Wilson IW, Chapple R, Dennis ES, Chaudhury A (2001) The Arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13:2115–2125
Hlouchova K, Navratil V, Tykvart J, Sacha P, Konvalinka J (2012) GCPII variants, paralogs and orthologs. Curr Med Chem 19:1316–1322
Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54
Huang W, Pitorre D, Poretska O, Marizzi C, Winter N, Poppenberger B, Sieberer T (2015) ALTERED MERISTEM PROGRAM1 suppresses ectopic stem cell niche formation in the shoot apical meristem in a largely cytokinin-independent manner. Plant Physiol 167:1471–1486
Hülskamp M, Misra S, Jürgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566
Ingouff M, Jullien PE, Berger F (2006) The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18:3491–3501
Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063
Ishida T, Kurata T, Okada K, Wada TA (2008) Genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59:365–386
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39
Jofuku D, den Boer BGW, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225
Kieber JJ, Rotheberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72:1–20
Kong J, Lau S, Jurgens G (2015) Twin plants from supernumerary egg cells in Arabidopsis. Curr Biol 25:225–230
Koornneef M (1981) The complex syndrome of the ttg mutants. Arabid Inf Serv 18:45–51
Koornneef M, Dellaert LWM, Vanderveen JH (1982) EMS-induced and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L) heynh. Mutat Res 93:109–123
Lafon C, Köhler C (2014) Embryo and endosperm, partners in seed development. Curr Opin Plant Biol 17:64–69
Lau S, Slane D, Herud O, Kong J, Jürgens G (2012) Early embryogenesis in flowering plants: settings up the basic body pattern. Annu Rev Plant Biol 63:483–506
Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771
Libault M, Brechenmacher L, Cheng J, Xu D, Stacey G (2010) Root hairs systems biology. Trends Plant Sci 15:641–650
Lin Y, Schiefelbein J (2001) Embryonic control of epidermal cell patterning in the root and hypocotyl of Arabidopsis. Development 128:3697–3705
Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M, Gao Q, Tian LL, Xu ZH, Bao F, Hu Y, Ye NS, Pei ZM, He YK (2013) Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc Natl Acad Sci U S A 110:1548–1553
Locascio A, Roig-Villanova I, Bernardi J, Varotto S (2014) Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Front Plant Sci 5:1–22
López-Bucio JS, Dubrovsky JG, Raya-González J, Ugartechea-Chirino Y, López-Bucio J, de Luna-Valdez LA, Ramos-Vega M, León P, Guevara-García AA (2014) Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J Exp Bot 65:169–183
Lukowitz W, Roeder A, Parmenter D, Somerville C (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116:109–119
Masucci JD, Rerie WG, Foreman DR, Zhang M, Galway ME, Marks MD, Schiefelbein JW (1996) The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122:1252–1260
Mordhorst AP, Voerman KJ, Hartog MV, Meijer EA, van Went J, Koornneef M, de Vries SC (1998) Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. Genetics 149:549–563
Morquecho-Contreras A, Méndez-Bravo A, Pelagio-Flores R, Raya-González J, Ortíz-Castro R, López-Bucio J (2010) Characterization of drr1, an alkamide-resistant mutant of Arabidopsis, reveals an important role for small lipid amides in lateral root development and plant senescence. Plant Physiol 152:1659–1673
Nambara E, Naito S, McCourt P (1992) A mutant of Arabidopsis which is defective in seed development and storage protein accumulation is a new abi3 allele. Plant J 2:435–441
Nambara E, Keith K, McCourt P, Naito S (1995) A regulatory role for the ABI3 gene in the establishment of embryo maturation in Arabidopsis thaliana. Development 121:629–636
Nogué F, Grandjean O, Craig S, Dennis E, Chaudhury AM (2000a) Higher level of cell proliferation rate and cyclin CycD3 expression in the Arabidopsis amp1 mutant. Plant Growth Regul 32:275–283
Nogué F, Hocart C, Letham DS, Dennis ES, Chaudhury AM (2000b) Cytokinin synthesis is higher in the Arabidopsis amp1 mutant. Plant Growth Regul 32:267–273
Okushima Y, Fukaki H, OnadaM Theologis A, Tasaka M (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–1340
Orozco-Arroyo G, Paolo D, Ezquer I, Colombo L (2015) Networks controlling seed size in Arabidopsis. Plant Reprod 28:17–32
Parcy F, Valon C, Kohara A, Miséra S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE 3 (ABI3), FUSCA 3 (FUS3) and LEAFY COTYLEDON 1 (LEC1) loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277
Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M (2009) Complex regulation of the TIR/AFB family of auxin receptors. Proc Natl Acad Sci USA 106:22540–22545
Pattanaik S, Patra B, Kumar S, Yuan L (2014) An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis. Front Plant Sci 5:1–8
Pickett FB, Wilson AK, Estelle M (1990) The aux1 mutation of Arabidopsis confers both auxin and ethylene resistance. Plant Physiol 94:1462–1466
Raya-González J, Ortiz-Castro R, Ruiz-Herrera LF, Kazan K, López-Bucio J (2014) Phytochrome and flowering time1/mediator25 regulates lateral root formation via auxin signaling in Arabidopsis. Plant Physiol 165:880–894
Rerie WG, Feldman DD, Carrington JC (1994) The GLABRA2 gene encodes a homeodomain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399
Roszak P, Köhler C (2011) Polycomb group proteins are required to couple seed coat initiation to fertilization. Proc Natl Acad Sci USA 108:20826–20832
Ruiz-Herrera LF, Shane M, López-Bucio J (2015) Nutritional regulation of root development. Wires Dev Biol 4:431–443
Saibo NJ, Vriezen WH, De Grauwe L, Azmi A, Prinsen E, Van Der Straeten D (2007) A comparative analysis of the Arabidopsis mutant amp1-1 and a novel weak amp1 allele reveals new functions of the AMP1 protein. Planta 225:831–842
Schiefelbein J (2003) Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr Opin Plant Biol 6:74–78
Shi H, Ye T, Wang Y, Chan Z (2013a) Arabidopsis ALTERED MERISTEM PROGRAM 1 negatively modulates plant responses to abscisic acid and dehydration stress. Plant Physiol Biochem 67:209–216
Shi Y, Wang Z, Meng P, Tian S, Zhang X, Yang S (2013b) The glutamate carboxypeptidase AMP1 mediates abscisic acid and abiotic stress responses in Arabidopsis. New Phytol 199:135–150
Smalle J, Kurepa J, Yang P, Babiychuk E, Kushnir S, Durski A, Vierstra RD (2002) Cytokinin growth responses in Arabidopsis involve the 26S proteasome subunit RPN12. Plant Cell 14:17–32
Tiryaki I, Staswick P (2002) An Arabidopsis mutant defective in jasmonate response is allelic to the auxin-signaling mutant axr1. Plant Physiol 130:887–894
Tominaga-Wada R, Iwata M, Sugiyama J, Katoke T, Ishida T, Yokoyama R, Nishitani K, Kiyotaka Okada, Wada T (2009) The GLABRA2 hoeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis Roots. Plant J 60:564–574
Ueguchi C, Koizumi H, Suzuki T, Mizuno T (2001) Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–235
Ullah H, Chen JG, Wang S, Jones AM (2002) Role of a heterotrimeric G protein in regulation of Arabidopsis seed germination. Plant Physiol 129:897–907
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
Vidaurre DP, Ploense S, Krogan NT, Berleth T (2007) AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 134:2561–2567
Voiniciuc C, Yang B, Schmidt MHW, Günl M, Usadel B (2015) Starting to gel: how Arabidopsis seed coat epidermal cells produce specialized secondary cell walls. Int J Mol Sci 16:3452–3473
Volodymyr R, Boriskuj L (2014) Physical, metabolic and developmental functions of the seed coat. Front Plant Sci 5:1–17
Walker AR, Davidson PA, Bolognesi-Winfield AC, James CM, Srinivasan N, Blundellb TL, Esche JJ, Marks MD, Gray JC (1999) The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11:1337–1350
Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73
Western TL, Burn J, Skinner DJ, Martin-McCaffrey L, Moffatt BA, Haughn GW (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol 127:998–1011
Western TL, Young DS, Dean GH, Tan WL, Samuels AL, Haughn GW (2004) MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in Arabidopsis seed coat. Plant Physiol 134:296–306
Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239:289–297
Wilson AK, Pickett FB, Turner JC, Estelle M (1990) A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol Gen Genet 222:377–383
Windsor J, Symonds V, Mendenhall J, Lloyd A (2000) Arabidopsis seed coat development: morphological differentiation of the outer integument. Plant J 22:483–493
Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis mutant that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol 119:521–530
Yao Y, Dong CH, Yi Y, Li X, Zhang X, Liu J (2014) Regulatory function of AMP1 in ABA biosynthesis and drought resistance in Arabidopsis. J Plant Biol 57:117–126
Zhou Z, Wang L, Li J, Song X, Yang C (2009) Study on programmed cell death and dynamic changes of starch accumulation in pericarp cells of Triticum aestivum L. Protoplasma 236:49–58
Zürcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr P, Müller B (2013) A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161:1066–1075
Acknowledgments
We are thankful to the Arabidopsis stock center for kindly providing us with Arabidopsis mutant seeds and Jose Antonio Rodríguez-Torres and Víctor López-Morelos for permission and advice for the use of electronic microscope, and León F. Ruiz-Herrera for support in confocal imaging. Drs. Shuhua Yang, Tom Guilfoyle, Bruno Müller, and Patricia León are thanked for providing us Arabidopsis mutant and transgenic lines. This work was supported by grants from the Consejo Nacional de Ciencia y Tecnología (CONACYT, México, Grant no. 177775), the Consejo de la Investigación Científica (UMSNH, México, Grant No. CIC 2.26), and the UNAM-DGAPA-PAPIIT (Grant IN207014 to AAGG and JSLB).
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López-García, C.M., Raya-González, J., López-Bucio, J.S. et al. ALTERED MERISTEM PROGRAM 1 Plays a Role in Seed Coat Development, Root Growth, and Post-Embryonic Epidermal Cell Elongation in Arabidopsis . J Plant Growth Regul 35, 1141–1158 (2016). https://doi.org/10.1007/s00344-016-9612-3
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DOI: https://doi.org/10.1007/s00344-016-9612-3