Abstract
Main conclusion
Arabidopsis Mediator subunits 2, 14, 15a, 16, and 25 are required for papillae development on the trichome cell wall surface.
Arabidopsis leaf hairs exhibit raised protrusions, termed papillae, on their cell wall surfaces. Here, we show that the glassy hair mutant, glh2, exhibits trichomes with an approximate 11-fold decrease in papillae density on their surfaces in comparison to wild type. This phenotype was found to be the result of mutations in Arabidopsis Mediator subunit 16. MED16 is localized to the nucleus of trichomes, consistent with Mediator’s role in transcription. The expression patterns of the trichome development reporters, ETR2pro::GUS and GL2pro::GUS, as well as GL2 transcript levels were not altered in the glh2 mutant. Screening of available T-DNA insertion lines in other subunits of the Mediator tail module revealed glassy trichome phenotypes in med2, med14, and med15a mutants. The data suggest that the Mediator complex is required for expression of genes involved in trichome papillae development.
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References
Bischoff V, Nita S, Neumetzler L, Schindelasch D, Urbain A, Eshed R, Persson S, Delmer D, Scheible WR (2010) Trichome birefringence and its homolog At5g01360 encode novel plant-specific DUF231 proteins required for cellulose biosynthesis in Arabidopsis thaliana. Plant Physiol 153:590–602
Cai G, Imasaki T, Takagi Y, Asturias FJ (2009) Mediator structural conservation and implications for the regulation mechanism. Structure 17:559–567
Canet JV, Dobón A, Tornero P (2012) Non-recognition-of-BTH4, an Arabidopsis mediator subunit homolog, is necessary for development and response to salicylic acid. Plant Cell 24:4220–4235
Cevher MA, Shi Y, Li D, Chait BT, Malik S, Roeder RG (2014) Reconstitution of active human core Mediator complex reveals a critical role of the MED14 subunit. Nat Struct Mol Biol 21:1028–1034
Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469
Dotson MR, Yuan CX, Roeder RG, Myers LC, Gustafsson CM, Jiang YW, Li Y, Kornberg RD, Asturias FJ (2000) Structural organization of yeast and mammalian mediator complexes. Proc Natl Acad Sci USA 97:14307–14310
Folkers U, Berger J, Hulskamp M (1997) Cell morphogenesis of trichomes in Arabidopsis: differential control of primary and secondary branching by branch initiation regulators and cell growth. Development 124:3779–3786
Fornero C, Suo B, Zahde M, Juveland K, Kirik V (2017) Papillae formation on trichome cell walls requires the function of the mediator complex subunit Med25. Plant Mol Biol 95:389–398
Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863
Hemsley PA, Hurst CH, Kaliyadasa E, Lamb R, Knight MR, De Cothi EA, Steele JF, Knight H (2014) The Arabidopsis mediator complex subunits MED16, MED14, and MED2 regulate mediator and RNA polymerase II recruitment to CBF-responsive cold-regulated genes. Plant Cell 26:465–484
Hülskamp M, Miséra S, Jürgens G (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76:555–566
Jakoby MJ, Falkenhan D, Mader MT, Brininstool G, Wischnitzki E, Platz N, Hudson A, Hülskamp M, Larkin J, Schnittger A (2008) Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-like transcriptional regulator MYB106. Plant Physiol 148:1583–1602
Jeronimo C, Robert F (2017) The mediator complex: at the nexus of RNA Polymerase II transcription. Trends Cell Biol 27:765–783
Knight H, Veale EL, Warren GJ, Knight MR (1999) The sfr6 mutation in Arabidopsis suppresses low-temperature induction of genes dependent on the CRT/DRE sequence motif. Plant Cell 11:875–886
Knight H, Thomson AJ, McWatters HG (2008) Sensitive to freezing 6 integrates cellular and environmental inputs to the plant circadian clock. Plant Physiol 148:293–303
Knight H, Mugford SG, Ülker B, Gao D, Thorlby G, Knight MR (2009) Identification of SFR6, a key component in cold acclimation acting post-translationally on CBF function. Plant J 58:97–108
Le J, El-Assal SE, Basu D, Saad ME, Szymanski DB (2003) Requirements for Arabidopsis ATARP2 and ATARP3 during epidermal development. Curr Biol 13:1341–1347
Lukowitz W, Gillmor CS, Scheible WR (2000) Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you. Plant Physiol 123:795–805
Madson M, Dunand C, Li X, Verma R, Vanzin GF, Caplan J, Shoue DA, Carpita NC, Reiter WD (2003) The MUR3 gene of Arabidopsis encodes a xyloglucan galactosyltransferase that is evolutionarily related to animal exostosins. Plant Cell 15:1662–1670
Malik S, Molina H, Xue Z (2017) PIC activation through functional interplay between mediator and TFIIH. J Mol Biol 429:48–63
Marks MD (1997) Molecular genetic analysis of trichome development in Arabidopsis. Annu Rev Plant Physiol Plant Mol Biol 48:137–163
Marks MD, Gilding E, Wenger JP (2007) Genetic interaction between glabra3-shapeshifter and siamese in Arabidopsis thaliana converts trichome precursors into cells with meristematic activity. Plant J 52:352–361
Marks MD, Wenger JP, Gilding E, Jilk R, Dixon RA (2009) Transcriptome analysis of Arabidopsis wild-type and gl3–sst sim trichomes identifies four additional genes required for trichome development. Mol Plant 2:803–822
Mathur S, Vyas S, Kapoor S, Tyagi AK (2011) The mediator complex in plants: structure, phylogeny and expression profiling of representative genes in a dicot (Arabidopsis thaliana) and a monocot (Oryza sativa) during reproduction and abiotic stress. Plant Physiol 157:1609–1627
Meinke DW, Cherry JM, Dean C, Rounsley SD, Koornneef M (1998) Arabidopsis thaliana: a model plant for genome analysis. Science 282:662–682
Plaschka C, Lariviere L, Wenzeck L, Seizl M, Hemann M, Tegunov D, Petrotchenko EV, Borchers CH, Baumeister W, Herzog F, Villa E (2015) Architecture of the RNA polymerase II–mediator core initiation complex. Nature 518:376–380
Plett JM, Mathur J, Regan S (2009) Ethylene receptor ETR2 controls trichome branching by regulating microtubule assembly in Arabidopsis thaliana. J Exp Bot 60:3923–3933
Potikha T, Delmer DP (1995) A mutant of Arabidopsis thaliana displaying altered patterns of cellulose deposition. Plant J 7:453–460
Rerie WG, Feldmann KA, Marks MD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8:1388–1399
Robinson PJ, Trnka MJ, Bushnell DA, Davis RE, Mattei PJ, Burlingame AL, Kornberg RD (2016) Structure of a complete mediator-RNA polymerase II pre-initiation complex. Cell 166:1411–1422
Samanta S, Thakur JK (2015) Importance of mediator complex in the regulation and integration of diverse signaling pathways in plants. Front Plant Sci 6:757. https://doi.org/10.3389/fpls.2015.00757
Sorek N, Szemenyei H, Sorek H, Landers A, Knight H, Bauer S, Wemmer DE, Somerville CR (2015) Identification of mediator 16 as the Arabidopsis Cobra suppressor Mongoose 1. Proc Natl Acad Sci USA 112:16048–16053
Suo B, Seifert S, Kirik V (2013) Arabidopsis glassy hair genes promote tichome papillae development. J Exp Bot 64:4981–4991
Szymanski DB, Jilk RA, Pollock SM, Marks MD (1998) Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125:1161–1171
Szymanski DB, Marks MD, Wick SM (1999) Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11:2331–2347
Tsai KL, Tomomori-Sato C, Sato S, Conaway RC, Conaway JW, Asturias FJ (2014) Subunit architecture and functional modular rearrangements of the transcriptional mediator complex. Cell 157:1430–1444
Tsai KL, Yu X, Gopalan S, Chao TC, Zhang Y, Florens L, Washburn MP, Murakami K, Conaway RC, Conaway JW, Asturias FJ (2017) Mediator structure and rearrangements required for holoenzyme formation. Nature 544:196–201
Vanzin GF, Madson M, Carpita NC, Raikhel NV, Keegstra K, Reiter WD (2002) The mur2 mutant of Arabidopsis thaliana lacks fucosylated xyloglucan because of a lesion in fucosyltransferase AtFUT1. Proc Natl Acad Sci USA 99:3340–3345
Wang C, Yao J, Du X, Zhang Y, Sun Y, Rollins J, Mou Z (2015) The Arabidopsis mediator complex subunit16 is a key component of basal resistance against the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Plant Physiol 169:856–872
Wang C, Du X, Mou Z (2016) The mediator complex subunits MED14, MED15, and MED16 are involved in defense signaling crosstalk in Arabidopsis. Front Plant Sci 7:1947. https://doi.org/10.3389/fpls.2016.01947
Warren G, McKown R, Marin A, Teutonico R (1996) Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L.) Heynh. Plant Physiol 111:1011–1019
Wathugala DL, Hemsley PA, Moffat CS, Cremelie P, Knight MR, Knight H (2012) The Mediator subunit SFR6/MED16 controls defense gene expression mediated by salicylic acid and jasmonate responsive pathways. New Phytol 195:217–230
Xu R, Li Y (2011) Control of final organ size by mediator complex subunit 25 in Arabidopsis thaliana. Development 138:4545–4554
Yang Y, Ou B, Zhang J, Si W, Gu H, Qin G, Qu LJ (2014) The Arabidopsis mediator subunit MED16 regulates iron homeostasis by associating with EIN3/EIL1 through subunit MED25. Plant J 77:838–851
Yang Y, Li L, Qu LJ (2016) Plant mediator complex and its critical functions in transcription regulation. J Integr Plant Biol 58:106–118
Zhang X, Wang C, Zhang Y, Sun Y, Mou Z (2012) The Arabidopsis Mediator complex subunit16 positively regulates salicylate-mediated systemic acquired resistance and jasmonate/ethylene-induced defense pathways. Plant Cell 24:4294–4309
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
The authors would like to thank Dr. Heather Knight at Durham University, England, for kindly sending them 35S::GFP:MED16 seeds and the pK7WGF2 plasmid containing MED16 cDNA. They would like to acknowledge the Arabidopsis Biological Resource Center (http://abrc.osu.edu), from which they obtained T-DNA lines. Dr. Zhonglin Mou at University of Florida and Dr. Clint Chapple at Purdue University graciously sent them med14-1 & med15a, and med2-1, med3-1, med5a/med5b, & med23-4 seeds, respectively. The authors would also like to thank Dr. Martha Cook for her help with the SEM imaging. This research was supported by Illinois State University (CF, TR, and VK) and by a Weigel Grant from the Beta Lambda chapter of Phi-Sigma Biological Society awarded to CF.
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Fornero, C., Rickerd, T. & Kirik, V. Papillae formation on Arabidopsis leaf trichomes requires the function of Mediator tail subunits 2, 14, 15a, 16, and 25. Planta 249, 1063–1071 (2019). https://doi.org/10.1007/s00425-018-3063-y
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DOI: https://doi.org/10.1007/s00425-018-3063-y