Abstract
Observation of a differential expression pattern, including strong expression in meristematic tissue of an Agave tequilana GlsA/ZRF ortholog suggested an important role for this gene during bulbil formation and developmental changes in this species. In order to better understand this role, the two GlsA/ZFR orthologs present in the genome of Arabidopsis thaliana were functionally characterized by analyzing expression patterns, double mutant phenotypes, promoter-GUS fusions and expression of hormone related or meristem marker genes. Patterns of expression for A. thaliana show that GlsA/ZFR genes are strongly expressed in SAMs and RAMs in mature plants and developing embryos and double mutants showed multiple changes in morphology related to both SAM and RAM tissues. Typical double mutants showed stunted growth of aerial and root tissue, formation of multiple ectopic meristems and effects on cotyledons, leaves and flowers. The KNOX genes STM and BP were overexpressed in double mutants whereas CLV3, WUSCHEL and AS1 were repressed and lack of AtGlsA expression was also associated with changes in localization of auxin and cytokinin. These results suggest that GlsA/ZFR is an essential component of the machinery that maintains the integrity of SAM and RAM tissue and underline the potential to identify new genes or gene functions based on observations in non-model plants.
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References
Abraham Juarez MJ, Hernandez Cardenas R, Santoyo Villa JN, OʼConnor D, Sluis A, Hake S, Ordaz-Ortiz J et al (2015) Functionally different PIN proteins control auxin flux during bulbil development in Agave tequilana. J Exp Bot 66:3893–3905
Abraham-Juárez MJ, Martínez-Hernández A, Leyva-González MA, Luis Herrera-Estrella L, Simpson J (2010) Class I KNOX genes are associated with organogenesis during bulbil formation in Agave tequilana. J Exp Bot 61:4055–4067
Aloia L, Gutierrez A, Caballero JM, Croce LD (2015a) Direct interaction between Id 1 and Zrf 1 controls neural differentiation of embryonic stem cells. EMBO Rep 16:63–70
Aloia L, Demajo S, Di Croce L (2015b) ZRF1: a novel epigenetic regulator of stem cell identity and cancer. Cell Cycle 14:510–515
Arizaga S, Ezcurra E (1995) Insurance against reproductive failure in a semelparous plant: bulbil formation in Agave macroacantha flowering stalks. Oecologia 101:329–334
Arizaga S, Ezcurra E (2002) Propagation mechanisms in Agave macroacantha (Agavaceae), a tropical arid-land succulent rosette. Am J Bot 89:632–641
Berleth T, Jurgens G (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118:575–587
Carles CC, Ha CM, Jun JH, Fiume E, Fletcher JC (2010) Analyzing shoot apical meristem development. Methods Mol Biol 655:105–129
Chen DH, Huang Y, Liu C, Ruan Y, Shen WH (2014) Functional conservation and divergence of J-domain-containing ZUO1/ZRF orthologs throughout evolution. Planta 239:1159–1173
Cheng Y, Dai X, Zhao Y (2006) Auxin biosynthesis by the YUC- CA favin monooxygenases controls the formation of foral organs and vascular tissues in Arabidopsis. Genes Dev 20:1790–1799
Cheng Y, Dai X, Zhao Y (2007) Auxin synthesized by the YUC- CA favin monooxygenases is essential for embryogenesis and leaf for- mation in Arabidopsis. Plant Cell 19:2430–2439
Clark G (1981) Staining procedures. Williams & Wilkins, Baltimore
Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT–PCR profling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specifc genes. Plant J 38:366–379
Delgado Sandoval SC, Abraham Juárez MJ, Simpson J (2012) Agave tequilana MADS genes show novel expression patterns in meristems, developing bulbils and floral organs. Sex Plant Reprod 25:11–26
Dhondt S, Coppens F, De Winter F, Swarup K, Merks RMH, Inzé D, Bennett MJ et al (2010) SHORT-ROOT and SCARECROW regulate leaf growth in Arabidopsis by stimulating S-phase progression of the cell cycle. Plant Physiol 154:1183–1195
Felsenstein J (1986) Jackknife, bootstrap and other resampling methods in regression-analysis—discussion. Ann Stat 14:1304–1305
Fiesselmann BS, Luichtl M, Yang X, Matthes M, Peis O, Torres-ruiz RA (2015) Ectopic shoot meristem generation in monocotyledonous rpk1 mutants is linked to SAM loss and altered seedling morphology. BMC Plant Biol. doi:10.1186/s12870-015-0556-8
Jackson D, Veit B, Hake S (1994) Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:405–413
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: b-glucoronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Karimi M, Inze D, Depicker A (2002) Gateway® vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195
Kaya H, Shibahara K, Taoka K, Iwabuchi M, Stillman B, Araki T (2001) FASCIATA genes for chromatin assembly factor-1 in arabidopsis maintain the cellular organization of apical meristems. Cell 104:131–142
Larkin MA, Blackshields G, Brown NP et al (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948
Marsch-Martínez N, Ramos-Cruz D, Reyes-Olalde JI, Lozano-Sotomayor P, Zúñiga-Mayo VM, de Folter S (2012) The role of cytokinin during Arabidopsis gynoecia and fruit morphogenesis and patterning. Plant J 72:222–234
Martínez-Trujillo M, Limones-Briones V, Cabrera-Ponce JL, Herrera-Estrella L (2004) Improving transformation efficiency of Arabidopsis thaliana by modifying the floral dip method. Plant Mol Biol Report 22:63–70
McBride KE, Summerfelt KR (1990) Improved binary vectors for Agrobacterium-mediated plant transformation. Plant Mol Biol 14:269–276
Miller SM, Kirk DL (1999) glsA, a Volvox gene required for asymmetric division and germ cell specification, encodes a chaperone-like protein. Development 126:649–658
Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2003) Identification of higher plant GlsA, a putative morphogenesis factor of gametic cells. Biochem Biophys Res Commun 306:564–569
Rajan VBV, DʼSilva P (2009) Arabidopsis thaliana J-class heat shock proteins: cellular stress sensors. Funct Integr Genom 9:433–446
Richly H, Rocha-Viegas L, Ribeiro JD, Demajo S, Gundem G, Lopez-Bigas N, Nakagawa T, Rospert S, Ito T, Di Croce L (2010) Transcriptional activation of polycomb-repressed genes by ZRF1. Nature 468:1124–1128
Ruiz-Medrano R, Xoconostle-Cazarez B, Lucas WJ (1999) Phloem long-distance transport of CmNACP mRNA: implications for supracelular regulation in plants. Development 126:4405–4419
Sang Y, Silva-Ortega CO, Wu S, Yamaguchi N, Wu MF, Pfluger J, Gillmor CS, Gallagher KL, Wagner D (2012) Mutations in two non-canonical Arabidopsis SWI2/SNF2 chromatin remodeling ATPases cause embryogenesis and stem cell maintenance defects. Plant J 72:1000–1014
Scofield S, Dewitte W, Murray JA (2014) STM sustains stem cell function in the Arabidopsis shoot apical meristem and controls KNOX gene expression independently of the transcriptional repressor AS1. Plant Signal Behav. doi:10.4161/psb.28934
Smith S, Stillman B (1989) CAF-I, a human cell factor required for chromatin assembly during DNA. Purification and characterization of replication in vitro. Cell 58:15–25
Su YH, Liu YB, Zhang XS (2011) Auxin-cytokinin interaction regulates meristem development. Mol Plant 4:616–625
Szarek SR, Driscoll B, Shohet C, Priebe S (1996) Bulbil production in Agave (Agavaceae) and related genera. Southwest Nat 41:465–469
Zúñiga-Mayo VM, Reyes-Olalde JI, Marsch-Martinez N, de Folter S (2014) Cytokinin treatments affect the apical-basal patterning of the Arabidopsis gynoecium and resemble the effects of polar auxin transport inhibition. Front Plant Sci 5:191
Acknowledgments
We are very grateful to Sarah Hake for critical reading of the manuscript and provision of experimental assistance and material in histological experiments. The STM::GUS line was kindly provided by Stewart Gillmor (Laboratorio Nacional de Genómica para la Biodiversidad LANGEBIO, CINVESTAV Irapuato). We also acknowledge the Arabidopsis Biological Resource Center and Marcos Castellanos (Nottingham Arabidopsis Stock Centre, University of Nottingham, Loughborough, UK) for provision of mutant seeds. J. A. G. L. and P. L. S. were supported by Mexican National Council of Science and Technology (CONACyT) fellowships (numbers 219888, and 219883, respectively). This work was carried out with financial support from CONACyT Grant No. 132160. We are grateful to Katia Gil Vega for technical assistance.
Author Contributions
J A. G. L. carried out the experiments, wrote and revised the paper, M. J. A. J. helped with the experiments and revised the paper, P. L. S. performed the analysis of SEM and revised the paper, S. D. F. coordinated the microscopic analysis of SEM and revised the paper, J. S. designed and coordinated the study and wrote and revised the paper. All authors reviewed the results and approved the final version of the manuscript.
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Guzmán-López, J.A., Abraham-Juárez, M.J., Lozano-Sotomayor, P. et al. Arabidopsis thaliana gonidialess A/Zuotin related factors (GlsA/ZRF) are essential for maintenance of meristem integrity. Plant Mol Biol 91, 37–51 (2016). https://doi.org/10.1007/s11103-016-0439-x
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DOI: https://doi.org/10.1007/s11103-016-0439-x