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Journal of Plant Research

, Volume 132, Issue 1, pp 117–129 | Cite as

Arabidopsis Group IIId ERF proteins positively regulate primary cell wall-type CESA genes

  • Laddawan Saelim
  • Nobuhiro Akiyoshi
  • Tian Tian Tan
  • Ayumi Ihara
  • Masatoshi Yamaguchi
  • Ko Hirano
  • Makoto Matsuoka
  • Taku DemuraEmail author
  • Misato OhtaniEmail author
Regular Paper

Abstract

The cell wall determines morphology and the environmental responses of plant cells. The primary cell wall (PCW) is produced during cell division and expansion, determining the cell shape and volume. After cell expansion, specific types of plant cells produce a lignified wall, known as a secondary cell wall (SCW). We functionally analyzed Group IIId Arabidopsis AP2/EREBP genes, namely ERF34, ERF35, ERF38, and ERF39, which are homologs of a rice ERF gene previously proposed to be related to SCW biosynthesis. Expression analysis revealed that these four genes are expressed in regions related to cell division and/or cell differentiation in seedlings (i.e., shoot apical meristems, the primordia of leaves and lateral roots, trichomes, and central cylinder of primary roots) and flowers (i.e., vascular tissues of floral organs and replums and/or valve margins of pistils). Overexpression of ERF genes significantly upregulated PCW-type, but not SCW-type, CESA genes encoding cellulose synthase catalytic subunits in Arabidopsis seedlings. Transient co-expression reporter analysis indicated that ERF35, ERF38, and ERF39 possess transcriptional activator activity, and that ERF34, ERF35, ERF38, and ERF39 upregulated the promoter activity of CESA1, a PCW-type CESA gene, through the DRECRTCOREAT elements, the core cis-acting elements known to be recognized by AP2/ERF proteins. Together, our findings show that Group IIId ERF genes are positive transcriptional regulators of PCW-type CESA genes in Arabidopsis and are possibly involved in modulating cellulose biosynthesis in response to developmental requirements and environmental stimuli.

Keywords

Cellulose CESA ERF Transcriptional regulation Primary cell wall 

Abbreviations

CESA

Cellulose synthase

ERF

Ethylene response factor

GUS

β-glucuronidase

LUC

Luciferase

NST

NAC SECONDARY WALL THICKENING PROMOTING FACTOR

PCW

Primary cell wall

SCW

Secondary cell wall

VND

VASCULAR-RELATED NAC-DOMAIN

YFP

Yellow fluorescent protein

Notes

Acknowledgements

We thank Dr. Geoffrey O. Wasteneys and Dr. Miki Fujita (University of British Columbia), Dr. Nobutaka Mitsuda (AIST, Japan), Dr. Arata Yoneda, Dr. Ko Kato, and Dr. Minoru Kubo (Nara Institute of Science and Technology, Japan) for their fruitful discussions, and Ms. Shizuka Nishida and Ms. Eriko Tanaka (Nara Institute of Science and Technology, Japan) for the technical support. This work was supported in part by Japan Society for the Promotion of Science (KAKENHI Grant Number 25291062 to T.D.), the Ministry of Education, Culture, Sports, Science, and Technology of Japan (Grant-in-Aid for Scientific Research on Innovative Areas “The Plant Cell Wall as Information Processing System” Grant numbers 25114520 and 15H01235 to M.O., 24114002 to T.D., “Plant-Structure Optimization Strategy” Grant numbers 18H05484 and 18H05489 to M.O. and T.D., and Grants-in-Aid from the NC-CARP project to T.D.), and the Exploratory Research for Advanced Technology (ERATO) from Japan Science and Technology Agency (JST) (Grant number JPMJER1602 to M.O.) and Japan Advanced Plant Science Network.

Supplementary material

10265_2018_1074_MOESM1_ESM.pdf (258 kb)
Supplementary material 1 (PDF 257 KB)

References

  1. Ambavaram MM, Krishnan A, Trijatmiko KR, Pereira A (2011) Coordinated activation of cellulose and repression of lignin biosynthesis pathways in rice. Plant Physiol 155:916–931CrossRefGoogle Scholar
  2. Bonaccorso O, Lee JE, Puah L, Scutt CP, Golz JF (2012) FILAMENTOUS FLOWER controls lateral organ development by acting as both an activator and a repressor. BMC Plant Biol 12:176CrossRefGoogle Scholar
  3. Cassan-Wang H, Goué N, Saidi MN, Legay S, Sivadon P, Goffner D, Grima-Pettenati J (2013) Identification of novel transcription factors regulating secondary cell wall formation in Arabidopsis. Front Plant Sci 11:189Google Scholar
  4. Chandler JW, Cole M, Flier A, Grewe B, Werr W (2007) The AP2 transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 34:1653–1662CrossRefGoogle Scholar
  5. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefGoogle Scholar
  6. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861CrossRefGoogle Scholar
  7. Diaz-Martin J, Almoguera C, Prieto-Dapena P, Espinosa JM, Jordano J (2005) Functional interaction between two transcription factors involved in the developmental regulation of a small heat stress protein gene promoter. Plant Physiol 139:1483–1494CrossRefGoogle Scholar
  8. Dietz KJ, Vogel MO, Viehhauser A (2010) AP2/EREBP transcription factors are part of gene regulatory networks and integrate metabolic, hormonal and environmental signals in stress acclimation and retrograde signaling. Protoplasma 245:3–14CrossRefGoogle Scholar
  9. Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought, high-salt- and cold-responsive gene expression. Plant J 33:751–763CrossRefGoogle Scholar
  10. Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol Plant 4:199–211CrossRefGoogle Scholar
  11. Endo H, Yamaguchi M, Tamura T, Nakano Y, Nishikubo N, Yoneda A, Kato K, Kubo M, Kajita S, Katayama Y, Ohtani M, Demura T (2015) Multiple classes of transcription factors regulate the expression of VASCULAR-RELATEDNAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant Cell Physiol 56:242–254CrossRefGoogle Scholar
  12. Gardiner JC, Taylor NG, Turner SR (2003) Control of cellulose synthase complex localization in developing xylem. Plant Cell 15:1740–1748CrossRefGoogle Scholar
  13. Hamann T (2015) The plant cell wall integrity maintenance mechanism-concepts for organization and mode of action. Plant Cell Physiol 56:215–223CrossRefGoogle Scholar
  14. Hamann T, Osborne E, Youngs HL, Misson J, Nussaume L, Somerville C (2004) Global expression analysis of CESA and CSL genes in Arabidopsis. Cellulose 11:279–286CrossRefGoogle Scholar
  15. Hao D, Ohme-Takagi M, Sarai A (1998) Unique mode of GCC box recognition by the DNA-binding domain of ethylene-responsive element-binding factor (ERF domain) in plants. J Biol Chem 273:26857–26861CrossRefGoogle Scholar
  16. Heyman J, Canher B, Bisht A, Christiaens F, De Veylder L (2018) Emerging role of the plant ERF transcription factors in coordinating wound defense responses and repair. J Cell Sci 131:jcs208215CrossRefGoogle Scholar
  17. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucl Acid Res 27:297–300CrossRefGoogle Scholar
  18. Hirano K, Aya K, Morinaka Y, Nagamatsu S, Sato Y, Antonio BA, Namiki N, Nagamura Y, Matsuoka M (2013a) Survey of genes involved in rice secondary cell wall formation through a co-expression network. Plant Cell Physiol 54:1803–1821CrossRefGoogle Scholar
  19. Hirano K, Kondo M, Aya K, Miyao A, Sato Y, Antonio BA, Namiki N, Nagamura Y, Matsuoka M (2013b) Identification of transcription factors involved in rice secondary cell wall formation. Plant Cell Physiol 54:1791–1802CrossRefGoogle Scholar
  20. Höfte H, Voxeur A (2017) Plant cell walls. Curr Biol 27:R865–R870CrossRefGoogle Scholar
  21. Jofuku KD, Boer BGW, Montagu MV, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225CrossRefGoogle Scholar
  22. Kawabe H, Ohtani M, Kurata T, Sakamoto T, Demura T (2018) Protein S-nitrosylation regulates xylem vessel cell differentiation in Arabidopsis. Plant Cell Physiol 59:17–29CrossRefGoogle Scholar
  23. Kawamura A, Koshida S, Takada S (2008) Activator-to-repressor conversion of T-box transcription factors by the Ripply family of Groucho/TLE-associated mediators. Mol Cell Biol 28:3236–3244CrossRefGoogle Scholar
  24. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50:347–363CrossRefGoogle Scholar
  25. Kim WC, Kim JY, Ko JH, Kang H, Kim J, Han KH (2014) AtC3H14, a plant-specific tandem CCCH zinc-finger protein, binds to its target mRNAs in a sequence-specific manner and affects cell elongation in Arabidopsis thaliana. Plant J 80:772–784CrossRefGoogle Scholar
  26. Ko JH, Jeon HW, Kim WC, Han KH (2014) The MYB46/MYB83-mediated transcriptional regulatory programme is a gate keeper of secondary wall biosynthesis. Ann Bot 114:1099–1107CrossRefGoogle Scholar
  27. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860CrossRefGoogle Scholar
  28. Kumar M, Turner S (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112:91–99CrossRefGoogle Scholar
  29. Kumar M, Campbell L, Turner S (2016) Secondary cell walls: biosynthesis and manipulation. J Exp Bot 67:515–531CrossRefGoogle Scholar
  30. Lasserre E, Jobet E, Llauro C, Delseny M (2008) AtERF38 (At2g35700), an AP2/ERF family transcription factor gene from Arabidopsis thaliana, is expressed in specific cell types of roots, stems and seeds that undergo suberization. Plant Physiol Biochem 46:1051–1061CrossRefGoogle Scholar
  31. Marsch-Martinez N, Greco R, Becker JD, Dixit S, Bergervoet JH, Karaba A, de Folter S, Pereira A (2006) BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol Biol 62:825–843CrossRefGoogle Scholar
  32. Mitsuda N, Ohme-Takagi M (2008) NAC transcription factors NST1 and NST3 regulate pod shattering in a partially redundant manner by promoting secondary wall formation after the establishment of tissue identity. Plant J 56:768–778CrossRefGoogle Scholar
  33. Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006CrossRefGoogle Scholar
  34. Mitsuda N, Iwase A, Yamamoto H, Yoshida M, Seki M, Shinozaki K, Ohme-Takagi M (2007) NAC transcription factors, NST1 and NST3, are key regulators of the formation of secondary walls in woody tissues of Arabidopsis. Plant Cell 19:270–280CrossRefGoogle Scholar
  35. Mutwil M, Ruprecht C, Giorgi FM, Bringmann M, Usadel B, Persson S (2009) Transcriptional wiring of cell wall-related genes in Arabidopsis. Mol Plant 2:1015–1024CrossRefGoogle Scholar
  36. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432CrossRefGoogle Scholar
  37. Nakano Y, Yamaguchi M, Endo H, Rejab NA, Ohtani M (2015) NAC-MYB-based transcriptional regulation of secondary cell wall biosynthesis in land plants. Front Plant Sci 6:288CrossRefGoogle Scholar
  38. Obayashi T, Aoki Y, Tadaka S, Kagaya Y, Kinoshita K (2018) ATTED-II in 2018: a plant coexpression database based on investigation of the statistical property of the mutual rank index. Plant Cell Physiol 59:e3CrossRefGoogle Scholar
  39. Ohme-Takagi M. Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182CrossRefGoogle Scholar
  40. Ohtani M, Demura T, Sugiyama M (2008) Differential requirement for the function of SRD2, an snRNA transcription activator, in various stages of plant development. Plant Mol Biol 66:303–314CrossRefGoogle Scholar
  41. Ohtani M, Morisaki K, Sawada Y, Sano R, Uy AL, Yamamoto A, Kurata T, Nakano Y, Suzuki S, Matsuda M, Hasunuma T, Hirai MY, Demura T (2016) Primary metabolism during biosynthesis of secondary wall polymers of protoxylem vessel elements. Plant Physiol 172:1612–1624CrossRefGoogle Scholar
  42. Persson S, Hairong W, Milne J, Grier O, Somerville C (2005) Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc Natl Acad Sci USA 102:8633–8638CrossRefGoogle Scholar
  43. Pré M, Atallah M, Champion A, Vos MD, Pieterse CMJ, Memelink J (2008) The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol 147:1347–1357CrossRefGoogle Scholar
  44. Qin F, Sakuma Y, Li J, Liu Q, Li YQ, Shinozaki K, Yamaguchi-Shinozaki K (2004) Cloning and functional analysis of a novel DREB1/CBF transcription factor involved in cold-responsive gene expression in Zea mays L. Plant Cell Physiol 45:1042–1052CrossRefGoogle Scholar
  45. Qin QL, Liu JG, Zhang Z, Peng RH, Xiong AS, Yao QH (2007) Isolation optimization and functional analysis of the cDNA encoding transcription factor RdreB1 in Oryza sativa L. Mol Breed 19:329–340CrossRefGoogle Scholar
  46. Rashotte AM, Mason MG, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2006) A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two component pathway. Proc Natl Acad Sci USA 103:11081–11085CrossRefGoogle Scholar
  47. Rasmussen PB, Holst B, Valentin-Hansen P (1996) Dual-function regulators: the cAMP receptor protein and the CytR regulator can act either to repress or to activate transcription depending on the context. Proc Natl Acad Sci USA 93:10151–10155CrossRefGoogle Scholar
  48. Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498CrossRefGoogle Scholar
  49. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GHH, Schindelman G, Song S, Baskin TI, Dupree P, Wasteneys GO, Benfey PN (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidylinositol-anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17:1749–1763CrossRefGoogle Scholar
  50. Ruprecht C, Persson S (2012) Co-expression of cell wall-related genes: new tools and insights. Front Plant Sci 3:1–7CrossRefGoogle Scholar
  51. Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T (2001) Role of the putative membrane-bound endo-1,4-β-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263CrossRefGoogle Scholar
  52. Schuetz M, Smith R, Ellis B (2013) Xylem tissue specification, patterning, and differentiation mechanisms. J Exp Bot 64:11–31CrossRefGoogle Scholar
  53. Skinner JS, von Zitzewitz J, Szucs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen TH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551CrossRefGoogle Scholar
  54. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78CrossRefGoogle Scholar
  55. Suzuki M, Ketterling MG, McCarty DR (2005) Quantitative statistical analysis of cis-regulatory sequences in ABA/VP1- and CBF/DREB1-regulated genes of Arabidopsis. Plant Physiol 139:437–447CrossRefGoogle Scholar
  56. Taylor NG (2007) Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites a potential role in regulating protein degradation. Plant Mol Biol 64:161–171CrossRefGoogle Scholar
  57. Taylor NG, Scheible WR, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–780CrossRefGoogle Scholar
  58. Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2540CrossRefGoogle Scholar
  59. Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR (2003) Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc Natl Acad Sci USA 100:1450–1455CrossRefGoogle Scholar
  60. Voxeur A, Höfte H (2016) Cell wall integrity signaling in plants: “To grow or not to grow that’s the question”. Glycobiology 26:950–960CrossRefGoogle Scholar
  61. Ward JM, Smith AM, Shah PK, Galanti SE, Yi H, Demianski AJ, Graaff E, Keller B, Neff MM (2006) A new role for the Arabidopsis AP2 transcription factor, LEAFY PETIOLE, in gibberellin-induced germination is revealed by the misexpression of a homologous gene, SOB2/DRN-LIKE. Plant Cell 18:29–39CrossRefGoogle Scholar
  62. Watanabe Y, Schneider R, Barkwill S, Gonzales-Vigil E, Hill JL Jr, Samuels AL, Persson S, Mansfield SD (2018) Cellulose synthase complexes display distinct dynamic behaviors during xylem transdifferentiation. Proc Natl Acad Sci USA 115:E6366–E6374CrossRefGoogle Scholar
  63. Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381407CrossRefGoogle Scholar
  64. Xie L, Yang C, Wang X (2011) Brassinosteroids can regulate cellulose biosynthesis by controlling the expression of CESA genes in Arabidopsis. J Exp Bot 62:4495–4506CrossRefGoogle Scholar
  65. Yamaguchi M, Kubo M, Fukuda H, Demura T (2008) Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 55:652–664CrossRefGoogle Scholar
  66. Yamaguchi M, Ohtani M, Mitsuda N, Kubo M, Ohme-Takagi M, Fukuda H, Demura T (2010) VND-INTERACTING2, a NAC domain transcription factor, negatively regulates xylem vessel formation in Arabidopsis. Plant Cell 22:1249–1263CrossRefGoogle Scholar
  67. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T (2011) VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 66:579–590CrossRefGoogle Scholar
  68. Zhong R, Demura T, Ye ZH (2006) SND1, a NAC domain transcription factor, is a key regulator of secondary wall synthesis in fibers of Arabidopsis. Plant Cell 18:3158–3170CrossRefGoogle Scholar
  69. Zhong R, Richardson EA, Ye ZH (2007a) The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell 19:2776–2792CrossRefGoogle Scholar
  70. Zhong R, Richardson EA, Ye ZH (2007b) Two NAC domain transcription factors, SND1 and NST1, function redundantly in regulation of secondary wall synthesis in fibers of Arabidopsis. Planta 225:1603–1611CrossRefGoogle Scholar
  71. Zuo J, Niu QW, Chua NH (2000) An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J 24:266–273CrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Laddawan Saelim
    • 1
  • Nobuhiro Akiyoshi
    • 1
  • Tian Tian Tan
    • 1
    • 3
  • Ayumi Ihara
    • 1
  • Masatoshi Yamaguchi
    • 1
    • 4
  • Ko Hirano
    • 2
  • Makoto Matsuoka
    • 2
  • Taku Demura
    • 1
    Email author
  • Misato Ohtani
    • 1
    Email author
  1. 1.Division of Biological Science, Graduate School of Science and TechnologyNara Institute of Science and TechnologyIkomaJapan
  2. 2.Bioscience and Biotechnology CenterNagoya UniversityNagoyaJapan
  3. 3.Centre for Research in Biotechnology for AgricultureUniversity of MalayaKuala LumpurMalaysia
  4. 4.Graduate School of Science and EngineeringSaitama UniversitySaitamaJapan

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