Abstract
Key message
Arabidopsis med12 and med13 mutants exhibit shoot and root phenotypes related to an altered auxin homeostasis. Sucrose supplementation reactivates both cell division and elongation in primary roots as well as auxin-responsive and stem cell niche gene expression in these mutants. An analysis of primary root growth of WT, med12, aux1-7 and med12 aux1 single and double mutants in response to sucrose and/or N-1-naphthylphthalamic acid (NPA) placed MED12 upstream of auxin transport for the sugar modulation of root growth.
Abstract
The MEDIATOR (MED) complex plays diverse functions in plant development, hormone signaling and biotic and abiotic stress tolerance through coordination of transcription. Here, we performed genetic, developmental, molecular and pharmacological analyses to characterize the role of MED12 and MED13 on the configuration of root architecture and its relationship with auxin and sugar responses. Arabidopsis med12 and med13 single mutants exhibit shoot and root phenotypes consistent with altered auxin homeostasis including altered primary root growth, lateral root development, and root hair elongation. MED12 and MED13 were required for activation of cell division and elongation in primary roots, as well as auxin-responsive and stem cell niche gene expression. Remarkably, most of these mutant phenotypes were rescued by supplying sucrose to the growth medium. The growth response of primary roots of WT, med12, aux1-7 and med12 aux1 single and double mutants to sucrose and application of auxin transport inhibitor N-1-naphthylphthalamic acid (NPA) revealed the correlation of med12 phenotype with the activity of the auxin intake permease and suggests that MED12 acts upstream of AUX1 in the root growth response to sugar. These data provide compelling evidence that MEDIATOR links sugar sensing to auxin transport and distribution during root morphogenesis.
Similar content being viewed by others
Abbreviations
- AU:
-
Arbitrary units
- CDK:
-
Cyclin dependent kinase
- GFP:
-
Green fluorescent protein
- IAA:
-
Indole-3-acetic acid
- LR:
-
Lateral root
- LRP:
-
Lateral root primordia
- MED:
-
Mediator
- NPA:
-
N-1-Naphthylphthalamic acid
- PI:
-
Propidium iodide
- PIN:
-
Pinformed
- PLT:
-
Plethora
- PR:
-
Primary root
- QC:
-
Quiescent center
- SHR:
-
Short root
- SCR:
-
Scarecrow
- TOR:
-
Target of rapamycin
- WT:
-
Wild-type
- YFP:
-
Yellow fluorescent protein
References
Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120
Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44
Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Spatiotemporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508
Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433
Ding Z, Friml J (2010) Auxin regulates distal stem cell differentiation in Arabidopsis roots. Proc Natl Acad Sci USA 107:12046–12051
Gallavotti A (2013) The role of auxin in shaping shoot architecture. J Exp Bot 64:2593–2608
Gewin V (2010) An underground revolution. Nature 466:552–553
Gillmor CS, Park MY, Smith MR, Pepitone R, Kerstetter RA, Poethig RS (2010) The MED12-MED13 module of Mediator regulates the timing of embryo patterning in Arabidopsis. Development 137:113–122
Gillmor CS, Silva-Ortega CO, Willmann MR, Buendía-Monreal M, Poething RS (2014) The Arabidopsis Mediator CDK8 module gene CCT(MED12) and GCT(MED13) are global regulators of development phase transitions. Development 141:4580–4589
Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567
Hong SK, Haldin CE, Lawson ND, Weinstein BM, Dawid IB, Hukriede NA (2005) The zebrafish kohtalo/trap230 gene is required for the development of the brain, neural crest, and pronephric kidney. Proc Natl Acad Sci USA 102:18473–18478
Imura Y, Kobayashi Y, Yamamoto S, Furutani M, Tasaka M, Abe M, Araki T (2012) CRYPTIC PRECOCIOUS/MED12 is a novel flowering regulator with multiple target steps in Arabidopsis. Plant Cell Physiol 53:287–303
Ito J, Sono T, Tasaka M, Furutani M (2011) MACCHI-BOU 2 is required for early embryo patterning and cotyledon organogenesis in Arabidopsis. Plant Cell Physiol 52:539–552
Ito J, Fukaki H, Onoda M, Li L, Li C, Tasaka M, Furutani M (2016) Auxin-dependent compositional change in Mediator in ARF7- and ARF19-mediated transcription. Proc Natl Acad Sci USA 113:6562–6567
Janody F, Martirosyan Z, Benlali A, Treisman JE (2003) Two subunits of the Drosophila Mediator complex act together to control cell affinity. Development 130:3691–3701
Kidd BN, Edgar CI, Kumar KK, Aitken EA, Schenk PM, Manners JM, Kazan K (2009) The Mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defense in Arabidopsis. Plant Cell 21:2237–2252
Kircher S, Schopfer P (2012) Photosynthetic sucrose acts as cotyledon derived long-distance signal to control root growth during early seedling development in Arabidopsis. Proc Natl Acad Sci USA 109:11217–11221
Koch KE (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246
Ljung K, Nemhauser JL, Perata P (2015) New mechanistic links between sugar and hormone signalling networks. Curr Opin Plant Biol 25:130–137
López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphorus availability alters root architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256
Lucas M, Swarup R, Paponov IA et al (2011) SHORT-ROOT regulates primary, lateral, and adventitious root development in Arabidopsis. Plant Physiol 155:384–398
MacGregor DR, Deak KI, Ingram PA, Malamy JE (2008) Root system architecture in Arabidopsis grown in culture is regulated by sucrose uptake in the aerial tissues. Plant Cell 20:2643–2660
Mähönen AP, Tusscher K, Siligato R, Smetana O, Diaz-Trivino S, Salojärvi J, Wachsman G, Heidstra R, Scheres B (2014) PLETHORA gradient formation mechanism separates auxin responses. Nature 515:125–129
Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44
Malik S, Roeder RG (2010) The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 11:761–772
Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–597
Pérez-Torres CA, López-Bucio J, Cruz-Ramírez A, Ibarra-Laclette E, Dharmasiri S, Estelle M, Herrera-Estrella L (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272
Petersson SV, Johansson AI, Kowalczyk M, Kakoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668
Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688
Puig J, Pauluzzi G, Guiderdoni E, Gantet P (2012) Regulation of shoot and root development through mutual signaling. Mol Plant 5:974–983
Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1908–1917
Rau MJ, Fischer S, Neumann CJ (2006) Zebrafish Trap230/Med12 is required as a coactivator for Sox9-dependent neural crest, cartilage and ear development. Dev Biol 296:83–93
Raya-González J, Ortiz-Castro R, Ruíz-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
Reyes-Hernández BJ, Srivastava AC, Ugartechea-Chirino Y et al (2014) The root indeterminacy-to-determinacy developmental switch is operated through a folate-dependent pathway in Arabidopsis thaliana. New Phytol 202:1223–1236
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709
Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:354–358
Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramírez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–178
Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354
Seguela-Arnaud M, Smith C, Castellanos-Uribe M, May S, Fisch H, McKenzie N, Bevan MW (2015) The Mediator complex subunits MED25/PFT1 and MED8 are required for transcriptional responses to changes in cell wall arabinose composition and glucose treatment in Arabidopsis thaliana. BMC Plant Biol 15:215
Skylar A, Sung F, Chory J, Wu X (2011) Metabolic sugar signal promotes Arabidopsis meristematic proliferation via G2. Dev Biol 351:82–89
Srivastava AC, Ramos-Parra PA, Bedair M, Robledo-Hernández AL, Tang Y, Sumner LW, Díaz de la Garza RI, Blancaflor EB (2011) The folylpolyglutamate synthetase plastidial isoform is required for postembryonic root development in Arabidopsis. Plant Physiol 155:1237–1251
Stepanova AN, Robertson-Hoyt J, Yun J, Benavente LM, Xie DY, Dolezal K, Schlereth A, Jürgens G, Alonso JM (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133:177–191
Stokes ME, Chattopadhyay A, Wilkins O, Nambara E, Campbell MM (2013) Interplay between sucrose and folate modulates auxin signaling in Arabidopsis. Plant Physiol 162:1552–1565
Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–2653
Treisman J (2001) Drosophila homologues of the transcriptional coactivation complex subunits TRAP240 and TRAP230 are required for identical processes in eye antennal disc development. Development 128:603–615
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
Van Norman JM, Xuan W, Beeckman T, Benfey PN (2013) To branch or not to branch: the role of pre-patterning in lateral root formation. Development 140:4301–4310
Wang L, Ruan YL (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci 4:1–9
Woodward A, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735
Xiong Y, McCormack M, Li L, Hall Q, Xiang C, Sheen J (2013) Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496:181–186
Yoda A, Kouike H, Okano H, Sawa H (2005) Components of the transcriptional Mediator complex are required for asymmetric cell division in C. elegans. Development 132:1885–1893
Zhang Y, Wu H, Wang N, Fan H, Chen C, Cui Y, Liu H, Ling HQ (2014) Mediator subunit 16 functions in the regulation of iron uptake gene expression in Arabidopsis. New Phytol 203:770–783
Acknowledgements
We are thankful to the Arabidopsis stock center for kindly providing us with Arabidopsis mutant seeds. Drs. Tom Guilfoyle, Ben Scheres, Philip N. Benfey, Stewart Gillmor and Alfredo Cruz Ramírez 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).
Author information
Authors and Affiliations
Contributions
JLB, JRG, LFRH, JCPR conceived and performed experiments. JRG, JLB wrote the manuscript. AAG, JSLB conceived and performed experiments and provided feedback. JLB and AAG repeatedly applied for funding.
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Raya-González, J., López-Bucio, J.S., Prado-Rodríguez, J.C. et al. The MEDIATOR genes MED12 and MED13 control Arabidopsis root system configuration influencing sugar and auxin responses. Plant Mol Biol 95, 141–156 (2017). https://doi.org/10.1007/s11103-017-0647-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-017-0647-z