PtrGH9A7, a poplar β-type endo-1,4-β-glucanase gene induced by auxin, promotes both plant growth and lateral root development by enhancing cell expansion.
Endo-1,4-β-glucanase (EGase) family genes function in multiple aspects of plant growth and development. Our previous study found that PtrCel9A6, a poplar EGase gene of the β subfamily, is specifically expressed in xylem tissue and is involved in the cellulose biosynthesis required for secondary cell wall formation (Yu et al. in Mol Plant 6:1904–1917, 2013). To further explore the functions and regulatory mechanism of β-subfamily EGases, we cloned and characterized another poplar β-type EGase gene PtrGH9A7, a close homolog of PtrCel9A6. In contrast to PtrCel9A6, PtrGH9A7 is predominantly expressed in parenchyma tissues of the above-ground part; in roots, PtrGH9A7 expression is specifically restricted to lateral root primordia at all stages from initiation to emergence and is strongly induced by auxin application. Heterologous overexpression of PtrGH9A7 promotes plant growth by enhancing cell expansion, suggesting a conserved role for β-type EGases in 1,4-β-glucan chains remodeling, which is required for cell wall loosening. Moreover, the overexpression of PtrGH9A7 significantly increases lateral root number, which might result from improved lateral root primordium development due to enhanced cell expansion. Taken together, these results demonstrate that this β-type EGase induced by auxin signaling has a novel role in promoting lateral root formation as well as in enhancing plant growth.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Lateral root primordium
Boer DR, Freire-Rios A, van den Berg WA, Saaki T, Manfield IW, Kepinski S, Lopez-Vidrieo I, Franco-Zorrilla JM, de Vries SC, Solano R, Weijers D, Coll M (2014) Structural basis for DNA binding specificity by the auxin-dependent ARF transcription factors. Cell 156:577–589
Boerjan W, Cervera MT, Delarue M, Beeckman T, Dewitte W, Bellini C, Caboche M, Van Onckelen H, Van Montagu M, Inze D (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419
Casimiro I, Marchant A, Bhalerao RP, Beeckman T, Dhooge S, Swarup R, Graham N, Inze D, Sandberg G, Casero PJ, Bennett M (2001) Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13:843–852
Catala C, Rose JK, Bennett AB (1997) Auxin regulation and spatial localization of an endo-1,4-beta-d-glucanase and a xyloglucan endotransglycosylase in expanding tomato hypocotyls. Plant J 12:417–426
Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9:2131–2142
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861
De Smet I, Tetsumura T, De Rybel B, Frei dit Frey N, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inze D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690
del Campillo E (1999) Multiple endo-1,4-beta-d-glucanase (cellulase) genes in Arabidopsis. Curr Top Dev Biol 46:39–61
Ferrarese L, Trainotti L, Moretto P, deLaureto PP, Rascio N, Casadoro G (1995) Differential ethylene-inducible expression of cellulase in pepper plants. Plant Mol Biol 29:735–747
Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inze D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351
Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Report 5:387–405
Koehler SM, Matters GL, Nath P, Kemmerer EC, Tucker ML (1996) The gene promoter for a bean abscission cellulase is ethylene-induced in transgenic tomato and shows high sequence conservation with a soybean abscission cellulase. Plant Mol Biol 31:595–606
Lashbrook CC, Gonzalez-Bosch C, Bennett AB (1994) Two divergent endo-beta-1,4-glucanase genes exhibit overlapping expression in ripening fruit and abscising flowers. Plant Cell 6:1485–1493
Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two-stage process. Development 121:3303–3310
Lau S, Jurgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746
Libertini E, Li Y, McQueen-Mason SJ (2004) Phylogenetic analysis of the plant endo-beta-1,4-glucanase gene family. J Mol Evol 58:506–515
Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44
Maloney VJ, Mansfield SD (2010) Characterization and varied expression of a membrane-bound endo-beta-1,4-glucanase in hybrid poplar. Plant Biotechnol J 8:294–307
Mølhøj M, Pagant S, Hofte H (2002) Towards understanding the role of membrane-bound endo-beta-1,4-glucanases in cellulose biosynthesis. Plant Cell Physiol 43:1399–1406
Ohmiya Y, Samejima M, Shiroishi M, Amano Y, Kanda T, Sakai F, Hayashi T (2000) Evidence that endo-1,4-beta-glucanases act on cellulose in suspension-cultured poplar cells. Plant J 24:147–158
Ohmiya Y, Nakai T, Park YW, Aoyama T, Oka A, Sakai F, Hayashi T (2003) The role of PopCel1 and PopCel2 in poplar leaf growth and cellulose biosynthesis. Plant J 33:1087–1097
Park YW, Tominaga R, Sugiyama J, Furuta Y, Tanimoto E, Samejima M, Sakai F, Hayashi T (2003) Enhancement of growth by expression of poplar cellulase in Arabidopsis thaliana. Plant J 33:1099–1106
Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408
Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2:a001446
Rose JK, Bennett AB (1999) Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4:176–183
Sato S, Kato T, Kakegawa K, Ishii T, Liu YG, Awano T, Takabe K, Nishiyama Y, Kuga S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1,4-beta-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263
Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954
Szyjanowicz PM, McKinnon I, Taylor NG, Gardiner J, Jarvis MC, Turner SR (2004) The irregular xylem 2 mutant is an allele of korrigan that affects the secondary cell wall of Arabidopsis thaliana. Plant J 37:730–740
Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868
Vilches-Barro A, Maizel A (2015) Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol 23:31–38
Wu SC, Blumer JM, Darvill AG, Albersheim P (1996) Characterization of an endo-beta-1,4-glucanase gene induced by auxin in elongating pea epicotyls. Plant Physiol 110:163–170
Yu L, Sun J, Li L (2013) PtrCel9A6, an endo-1,4-beta-glucanase, is required for cell wall formation during xylem differentiation in Populus. Mol Plant 6:1904–1917
Yu L, Chen H, Sun J, Li L (2014) PtrKOR1 is required for secondary cell wall cellulose biosynthesis in Populus. Tree Physiol 34:1289–1300
Yu L, Liu Y, Li Q, Tang G, Luo L (2016) Overexpression of phytosulfokine-alpha induces male sterility and cell growth by regulating cell wall development in Arabidopsis. Plant Cell Rep 35:2503–2512
We thank Ms. Jiqin Li at Shanghai Institute of Plant Physiology and Ecology for assistance with scanning electron microscopy. This work was supported by the National Natural Science Foundation of China (31500197, 31630014) and Shanghai Sailing Program (15YF1403800).
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Yu, L., Li, Q., Zhu, Y. et al. An auxin-induced β-type endo-1,4-β-glucanase in poplar is involved in cell expansion and lateral root formation. Planta 247, 1149–1161 (2018). https://doi.org/10.1007/s00425-018-2851-8
- Cell expansion
- Lateral root
- Lateral root primordium