The early inflorescence of Arabidopsis thaliana demonstrates positional effects in floral organ growth and meristem patterning

. 2018 Jun ; 31 (2) : 171-191. [epub] 20171220

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29264708

Grantová podpora
BB/E022618/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/J001295/1 Biotechnology and Biological Sciences Research Council - United Kingdom
P16508 Biotechnology and Biological Sciences Research Council - United Kingdom
Quota PhD studentship Biotechnology and Biological Sciences Research Council - United Kingdom

Odkazy

PubMed 29264708
PubMed Central PMC5940708
DOI 10.1007/s00497-017-0320-3
PII: 10.1007/s00497-017-0320-3
Knihovny.cz E-zdroje

Linear modelling approaches detected significant gradients in organ growth and patterning across early flowers of the Arabidopsis inflorescence and uncovered evidence of new roles for gibberellin in floral development. Most flowering plants, including the genetic model Arabidopsis thaliana, produce multiple flowers in sequence from a reproductive shoot apex to form a flower spike (inflorescence). The development of individual flowers on an Arabidopsis inflorescence has typically been considered as highly stereotypical and uniform, but this assumption is contradicted by the existence of mutants with phenotypes visible in early flowers only. This phenomenon is demonstrated by mutants partially impaired in the biosynthesis of the phytohormone gibberellin (GA), in which floral organ growth is retarded in the first flowers to be produced but has recovered spontaneously by the 10th flower. We presently lack systematic data from multiple flowers across the Arabidopsis inflorescence to explain such changes. Using mutants of the GA 20-OXIDASE (GA20ox) GA biosynthesis gene family to manipulate endogenous GA levels, we investigated the dynamics of changing floral organ growth across the early Arabidopsis inflorescence (flowers 1-10). Modelling of floral organ lengths identified a significant, GA-independent gradient of increasing stamen length relative to the pistil in the wild-type inflorescence that was separable from other, GA-dependent effects. It was also found that the first flowers exhibited unstable organ patterning in contrast to later flowers and that this instability was prolonged by exogenous GA treatment. These findings indicate that the development of individual flowers is influenced by hitherto unknown factors acting across the inflorescence and also suggest novel functions for GA in floral patterning.

Zobrazit více v PubMed

Aida M, Tasaka M. Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex. Plant Mol Biol. 2006;60:915–928. doi: 10.1007/s11103-005-2760-7. PubMed DOI

Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M. Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell. 1997;9:841–857. doi: 10.1105/tpc.9.6.841. PubMed DOI PMC

Airoldi CA. Determination of sexual organ development. Sex Plant Reprod. 2010;23:53–62. doi: 10.1007/s00497-009-0126-z. PubMed DOI

Bishop J, Jones HE, O’Sullivan DM, Potts SG. Elevated temperature drives a shift from selfing to outcrossing in the insect-pollinated legume, faba bean (Vicia faba) J Exp Bot. 2017;68:2055–2063. PubMed PMC

Blázquez MA, Green R, Nilsson O, Sussman MR, Weigel D. Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell. 1998;10:791–800. doi: 10.1105/tpc.10.5.791. PubMed DOI PMC

Bowman JA, Drews GN, Meyerowitz EM. Expression of the Arabidopsis floral homeotic gene AGAMOUS is restricted to specific cell types late in flower development. Plant Cell. 1991;3:749–758. doi: 10.1105/tpc.3.8.749. PubMed DOI PMC

Cardarelli M, Cecchetti V. Auxin polar transport in stamen formation and development: how many actors? Front Plant Sci. 2014;5:333. doi: 10.3389/fpls.2014.00333. PubMed DOI PMC

Cheng H, Qin L, Lee S, Fu X, Richards DE, Cao D, Luo D, Harberd NP, Peng J. Gibberellin regulates floral development via suppression of DELLA protein function. Development. 2004;131:1055–1064. doi: 10.1242/dev.00992. PubMed DOI

Cheng H, Song S, Xiao L, Soo HM, Cheng Z, Xie D, Peng J. Gibberellin acts through jasmonate to control the expression of MYB21, MYB24 and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet. 2009;5:e1000440. doi: 10.1371/journal.pgen.1000440. PubMed DOI PMC

Chiang H-H, Hwang I, Goodman HM. Isolation of the Arabidopsis GA4 locus. Plant Cell. 1995;7:195–201. doi: 10.1105/tpc.7.2.195. PubMed DOI PMC

Coen ES, Meyerowitz EM. The war of the whorls: genetic interactions controlling flower development. Nature. 1991;353:31–37. doi: 10.1038/353031a0. PubMed DOI

Coles JP, Phillips AL, Croker SJ, García-Lepe L, Lewis MJ, Hedden P. Modification of gibberellin production and plant development in Arabidopsis by sense and antisense expression of gibberellin 20-oxidase genes. Plant J. 1999;17:547–556. doi: 10.1046/j.1365-313X.1999.00410.x. PubMed DOI

De Storme N, Geelan D. The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant, Cell Environ. 2014;37:1–18. doi: 10.1111/pce.12142. PubMed DOI PMC

Dill A, Sun TP. Synergistic derepression of gibberellin signalling by removing RGA and GAI function in Arabidopsis thaliana. Genetics. 2001;159:777–785. PubMed PMC

Dill A, Jung SH, Sun TP. The DELLA motif is essential for gibberellin-induced degradation of RGA. Proc Natl Acad Sci USA. 2001;98:14162–14167. doi: 10.1073/pnas.251534098. PubMed DOI PMC

Fuentes S, Ljung K, Sorefan K, Alvey E, Harberd NP, Østergaard L. Fruit growth in Arabidopsis occurs via DELLA-dependent and DELLA-independent gibberellin responses. Plant Cell. 2012;24:3982–3996. doi: 10.1105/tpc.112.103192. PubMed DOI PMC

Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M. PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development. 2004;131:5021–5030. doi: 10.1242/dev.01388. PubMed DOI

Gomez KA, Gomez AA. Statistical procedures for agricultural research. New York: Wiley; 1984.

Gómez-Mena C, de Folter S, Costa MMR, Angenent GC, Sablowski R. Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development. 2005;132:429–438. doi: 10.1242/dev.01600. PubMed DOI

Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell. 2007;18:3399–3414. doi: 10.1105/tpc.106.047415. PubMed DOI PMC

Harberd N, Belfield E, Yasamura Y. The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell. 2009;21:1328–1339. doi: 10.1105/tpc.109.066969. PubMed DOI PMC

Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol. 2005;15:1434–1448. doi: 10.1016/j.cub.2005.09.052. PubMed DOI

Holtsford TP, Ellstrand NC. Genetic and environmental variation in floral traits affecting outcrossing rate in Clarkia tembloriensis (Onagraceae) Evolution. 1992;46:216–225. doi: 10.1111/j.1558-5646.1992.tb01996.x. PubMed DOI

Hu J, Mitchum MG, Barnaby N, et al. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell. 2008;20:320–336. doi: 10.1105/tpc.107.057752. PubMed DOI PMC

Huang S, Raman AS, Ream JE, Fujiwara H, Cerny RE, Brown SM. Overexpression of 20-oxidase confers a gibberellin-overproduction phenotype in Arabidopsis. Plant Physiol. 1998;118:773–781. doi: 10.1104/pp.118.3.773. PubMed DOI PMC

Irish VF. The flowering of Arabidopsis flower development. Plant J. 2010;61:1014–1028. doi: 10.1111/j.1365-313X.2009.04065.x. PubMed DOI

Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K. The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmoinc acid biosynthesis, which synchronises pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell. 2001;13:2191–2209. doi: 10.1105/tpc.13.10.2191. PubMed DOI PMC

Ito T, Ng KH, Lim TZ, Yu H, Meyerowitz EM. The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis. Plant Cell. 2007;19:3516–3529. doi: 10.1105/tpc.107.055467. PubMed DOI PMC

Itoh H, Tanaka-Ueguchi M, Kawaide H, Chen X, Kamiya Y, Matsuoka M. The gene encoding tobacco gibberellin 3β-hydroxylase is expressed at the site of GA action during stem elongation and flower organ development. Plant J. 1999;20:15–24. doi: 10.1046/j.1365-313X.1999.00568.x. PubMed DOI

Iuchi S, Susuki H, Kim YC, Iuchi A, Kuromori T, Ueguchi-Tanaka M, Asami T, Yamaguchi I, Matsuoka M, Kobayashi M, Nakajima M. Multiple loss-of-function of Arabidopsis gibberellin receptor AtGID1s completely shuts down a gibberellin signal. Plant J. 2007;50:958–966. doi: 10.1111/j.1365-313X.2007.03098.x. PubMed DOI

Jacobsen SE, Olszewski NE. Mutations in the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell. 1993;5:887–896. doi: 10.1105/tpc.5.8.887. PubMed DOI PMC

King KE, Moritz T, Harberd NP. Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics. 2001;159:767–776. PubMed PMC

Koornneef M, Van der Veen JH. Induction and analysis of gibberellin sensitive mutants in Arabidopsis thaliana (L) heyhn. Theor Appl Genet. 1980;58:257–263. doi: 10.1007/BF00265176. PubMed DOI

Laufs P, Coen E, Kronenberger J, Traas J, Doonan J. Separable roles of UFO during floral development revealed by conditional restoration of gene function. Development. 2003;130:785–796. doi: 10.1242/dev.00295. PubMed DOI

Levin JZ, Meyerowitz EM. UFO: An Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell. 1995;7:529–548. doi: 10.1105/tpc.7.5.529. PubMed DOI PMC

Levin JZ, Fletcher JC, Chen X, Meyerowitz EM. A genetic screen for modifiers of UFO meristem activity identifies three novel FUSED FLORAL ORGANS genes required for early flower development in Arabidopsis. Genetics. 1998;149:579–595. PubMed PMC

Li D, Guo Z, Liu C, Li J, Xu W, Chen Y. Quantification of near-attomole gibberellins in floral organs dissected from a single Arabidopsis flower. Plant J. 2017;91:547–557. doi: 10.1111/tpj.13580. PubMed DOI

McCullagh P, Nelder JA. Generalized linear models. London: Chapman and Hall; 1989.

Millar AA, Gublar F. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell. 2005;17:705–721. doi: 10.1105/tpc.104.027920. PubMed DOI PMC

Mishke JP, Brown JAM. Development of vegetative and floral meristems of Arabidopsis thaliana. Am J Bot. 1965;52:533–537. doi: 10.1002/j.1537-2197.1965.tb06818.x. DOI

Mitchum MG, Yamaguchi S, Hanada A, Kuwahara A, Yoshioka Y, Kato T, Tabata S, Kamiya Y, Sun TP. Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. Plant J. 2006;45:804–818. doi: 10.1111/j.1365-313X.2005.02642.x. PubMed DOI

Okamuro JK, Szeto W, Prass-Lotys C, Jofuku KD. Photo and hormonal control of meristem identity in the Arabidopsis flower mutants apetala2 and apetala1. Plant Cell. 1997;9:37–47. doi: 10.1105/tpc.9.1.37. PubMed DOI PMC

Otsuka M, Kenmoku H, Ogawa M, Okada K, Mitsuhashi W, Sassa T, Kamiya Y, Toyomasu T, Yamaguchi S. Emission of ent-kaurene, a diterpenoid hydrocarbon precursor for gibberellins, into the headspace from plants. Plant Cell Physiol. 2004;45:1129–1139. doi: 10.1093/pcp/pch149. PubMed DOI

Plackett ARG, Thomas SG, Wilson ZA, Hedden P. Gibberellin control of stamen development: a fertile field. Trends Plant Sci. 2011;16:568–578. doi: 10.1016/j.tplants.2011.06.007. PubMed DOI

Plackett ARG, Powers SJ, Fernandez-Garcia N, et al. Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1, -2 and -3 are the dominant paralogues. Plant Cell. 2012;24:941–960. doi: 10.1105/tpc.111.095109. PubMed DOI PMC

Plackett ARG, Ferguson AC, Powers SJ, Wanchoo-Kohli A, Phillips AL, Wilson ZA, Hedden P, Thomas SG. DELLA activity is required for successful pollen development in the Columbia ecotype of Arabidopsis. New Phytol. 2014;201:825–836. doi: 10.1111/nph.12571. PubMed DOI PMC

Prusinkiewicz P, Erasmus Y, Lane B, Harder LD, Coen E. Evolution and development of inflorescence architectures. Science. 2007;316:1452–1456. doi: 10.1126/science.1140429. PubMed DOI

Qin F, Kodaira KS, Maruyama K, Mizoi J, Tran LSP, Fujita Y, Morimoto K, Shinozaki K, Yamaguchi-Shinozaki K. SPINDLY, a negative regulator of gibberellic acid signalling, is involved in the plant abiotic stress response. Plant Physiol. 2011;157:1900–1913. doi: 10.1104/pp.111.187302. PubMed DOI PMC

Regnault T, Davière J-M, Wild M, Sakvarelidze-Achard L, Heintz D, Carrera Bergua E, Lopez Diaz I, Gong G, Hedden P, Achard P. The gibberellin precursor GA12 acts as a long-distance growth signal in Arabidopsis. Nat Plants. 2015;1:15073. doi: 10.1038/nplants.2015.73. PubMed DOI

Reinhardt D, Pesce ER, Stieger P, Mendel T, Baltensberger K, Bennett M, Traas J, Friml J, Kuhlemeier C. Regulation of phyllotaxis by polar auxin transport. Nature. 2003;426:255–260. doi: 10.1038/nature02081. PubMed DOI

Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, et al. The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis lifecycle. Plant J. 2008;53:488–504. doi: 10.1111/j.1365-313X.2007.03356.x. PubMed DOI

Sherry RA, Lord EM. A comparative developmental study of the selfing and outcrossing flowers of Clarkia tembloriensis (Onagraceae) Int J Plant Sci. 2000;161:563–574. doi: 10.1086/314286. DOI

Silverstone AL, Chang C-W, Krol E, Sun T-P. Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J. 1997;12:9–19. doi: 10.1046/j.1365-313X.1997.12010009.x. PubMed DOI

Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, Sun TP. Repressing a repressor: gibberell-ininduced rapid reduction of the RGA protein in Arabidopsis. Plant Cell. 2001;13:1555–1565. doi: 10.1105/tpc.13.7.1555. PubMed DOI PMC

Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell. 1990;2:755–767. doi: 10.1105/tpc.2.8.755. PubMed DOI PMC

Stintzi A, Browse J. The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA. 2000;97:10625–10630. doi: 10.1073/pnas.190264497. PubMed DOI PMC

Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP. DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol. 2004;135:1008–1019. doi: 10.1104/pp.104.039578. PubMed DOI PMC

Vivian-Smith A, Koltunow AM. Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol. 1999;121:437–451. doi: 10.1104/pp.121.2.437. PubMed DOI PMC

Wagner D, Sablowski RWM, Meyerowitz EM. Transcriptional activation of APETALA1 by LEAFY. Science. 1999;285:582–584. doi: 10.1126/science.285.5427.582. PubMed DOI

Wang Q, Hasson A, Rossmann S, Theres K. Divide et impera: boundaries shape the plant body and initiate new meristems. New Phytol. 2016;209:485–498. doi: 10.1111/nph.13641. PubMed DOI

Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EMN, Maier A, Schwechheimer C. The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell. 2007;19:1209–1220. doi: 10.1105/tpc.107.051441. PubMed DOI PMC

Yamaguchi S. Gibberellin metabolism and its regulation. Ann Rev Plant Biol. 2008;59:225–251. doi: 10.1146/annurev.arplant.59.032607.092804. PubMed DOI

Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D. Gibberellin acts positively then negatively to control the onset of flower formation in Arabidopsis. Science. 2014;344:638–641. doi: 10.1126/science.1250498. PubMed DOI

Yu H, Ito T, Zhao Y, Peng J, Kumar P, Meyerowitz EM. Floral homeotic genes are targets of gibberellin signalling in flower development. Proc Natl Acad Sci USA. 2004;101:7827–7832. doi: 10.1073/pnas.0402377101. PubMed DOI PMC

Zhao Y, Medrano L, Ohashi K, Fletcher JC, Yu H, Sakai H, Meyerowitz EM. HANABA TARANU is a GATA transcription factor that regulates shoot apical meristem and flower development in Arabidopsis. Plant Cell. 2004;16:2586–2600. doi: 10.1105/tpc.104.024869. PubMed DOI PMC

Zinn KE, Tunc-Ozdemier M, Harper JF. Temperature stress and plant sexual reproduction: uncovering the weakest links. J Exp Bot. 2010;61:1959–1968. doi: 10.1093/jxb/erq053. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...