, Volume 247, Issue 5, pp 1149–1161 | Cite as

An auxin-induced β-type endo-1,4-β-glucanase in poplar is involved in cell expansion and lateral root formation

  • Liangliang Yu
  • Qiong Li
  • Yingying Zhu
  • Muhammad Saddique Afzal
  • Laigeng Li
Original Article


Main conclusion

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.


Endo-1,4-β-glucanase Cell expansion Lateral root Lateral root primordium Auxin Poplar 







Lateral root


Lateral root primordium



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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

425_2018_2851_MOESM1_ESM.jpg (2.6 mb)
Supplementary material 1 (JPEG 2616 kb) Fig. S1 PtrGH9A7p:GUS is not induced by phytohormones except auxin. a-f Histochemical analyses of PtrGH9A7p:GUS seedlings treated with mock (a), 10 μM 2,4-D (b), GA3 (c), 6-BA (d), ABA (e), ACC (f) for 24 h. Bars = 2 mm
425_2018_2851_MOESM2_ESM.jpg (2.9 mb)
Supplementary material 2 (JPEG 3000 kb) Fig. S2 Representative images of LRPs at developmental stages II to emergence (a to g, respectively) and LRs (h and i) of 11-d-old wild-type and PtrGH9A7-OX transgenic seedlings


  1. 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 156:577–589CrossRefPubMedGoogle Scholar
  2. 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 7:1405–1419CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 13:843–852CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 12:417–426CrossRefPubMedGoogle Scholar
  5. Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9:2131–2142CrossRefPubMedGoogle Scholar
  6. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  7. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861CrossRefPubMedGoogle Scholar
  8. 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 134:681–690CrossRefPubMedGoogle Scholar
  9. del Campillo E (1999) Multiple endo-1,4-beta-d-glucanase (cellulase) genes in Arabidopsis. Curr Top Dev Biol 46:39–61CrossRefPubMedGoogle Scholar
  10. 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 29:735–747CrossRefPubMedGoogle Scholar
  11. 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 14:2339–2351CrossRefPubMedPubMedCentralGoogle Scholar
  12. Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Report 5:387–405CrossRefGoogle Scholar
  13. 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 31:595–606CrossRefPubMedGoogle Scholar
  14. 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 6:1485–1493PubMedPubMedCentralGoogle Scholar
  15. Laskowski MJ, Williams ME, Nusbaum HC, Sussex IM (1995) Formation of lateral root meristems is a two-stage process. Development 121:3303–3310PubMedGoogle Scholar
  16. Lau S, Jurgens G, De Smet I (2008) The evolving complexity of the auxin pathway. Plant Cell 20:1738–1746CrossRefPubMedPubMedCentralGoogle Scholar
  17. Libertini E, Li Y, McQueen-Mason SJ (2004) Phylogenetic analysis of the plant endo-beta-1,4-glucanase gene family. J Mol Evol 58:506–515CrossRefPubMedGoogle Scholar
  18. Malamy JE, Benfey PN (1997) Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44PubMedGoogle Scholar
  19. Maloney VJ, Mansfield SD (2010) Characterization and varied expression of a membrane-bound endo-beta-1,4-glucanase in hybrid poplar. Plant Biotechnol J 8:294–307CrossRefPubMedGoogle Scholar
  20. 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 43:1399–1406CrossRefPubMedGoogle Scholar
  21. 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 24:147–158CrossRefPubMedGoogle Scholar
  22. 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 33:1087–1097CrossRefPubMedGoogle Scholar
  23. 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 33:1099–1106CrossRefPubMedGoogle Scholar
  24. 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 14:399–408CrossRefPubMedGoogle Scholar
  25. Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. Cold Spring Harb Perspect Biol 2:a001446CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 4:176–183CrossRefPubMedGoogle Scholar
  27. 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 42:251–263CrossRefPubMedGoogle Scholar
  28. 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 10:946–954CrossRefPubMedGoogle Scholar
  29. 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 37:730–740CrossRefPubMedGoogle Scholar
  30. Ulmasov T, Hagen G, Guilfoyle TJ (1997) ARF1, a transcription factor that binds to auxin response elements. Science 276:1865–1868CrossRefPubMedGoogle Scholar
  31. Vilches-Barro A, Maizel A (2015) Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol 23:31–38CrossRefPubMedGoogle Scholar
  32. 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 110:163–170CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 6:1904–1917CrossRefPubMedGoogle Scholar
  34. Yu L, Chen H, Sun J, Li L (2014) PtrKOR1 is required for secondary cell wall cellulose biosynthesis in Populus. Tree Physiol 34:1289–1300CrossRefPubMedGoogle Scholar
  35. 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 35:2503–2512CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Shanghai Key Lab of Bio-energy Crops, School of Life SciencesShanghai UniversityShanghaiChina
  2. 2.National Key Laboratory of Plant Molecular Genetics and CAS Center for Excellence in Molecular Plant Sciences, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological SciencesChinese Academy of SciencesShanghaiChina

Personalised recommendations