pp 1–11 | Cite as

Specific roles of Os4BGlu10, Os6BGlu24, and Os9BGlu33 in seed germination, root elongation, and drought tolerance in rice

  • Ruijuan Ren
  • Dong Li
  • Chunyan Zhen
  • Defu ChenEmail author
  • Xiwen ChenEmail author
Original Article


Main conclusion

Morphological, physiological, and gene expression analyses showed that Os4BGlu10, Os6BGlu24, and Os9BGlu33 played specific roles in seed germination, root elongation, and drought tolerance of rice, with various relations with indole-3-acetic acid (IAA) and abscisic acid (ABA) signaling.

β-Glucosidases (BGlus) belong to glycoside hydrolase family 1 and have many functions in plants. In this study, we investigated the function of three BGlus in seed germination, drought tolerance, and root elongation using the loss-of-function mutants bglu10, bglu24, and bglu33. These mutants germinated slightly later under normal conditions and had significantly longer roots than the wild type. In the presence of ABA, bglu10 and bglu24 exhibited a higher germination inhibition percentage, whereas bglu33 had a lower germination inhibition percentage, compared to the wild type. All of the mutants exhibited less drought tolerance, with the survival rates significantly lower than that of the wild type, which was also confirmed by a decrease in relative leaf water content and Fv/Fm ratio after drought treatment. The root length of bglu10 did not respond to IAA, whereas that of bglu24 responded to a high (0.25 µM) concentration of IAA, and that of bglu33 to a low (0.05 µM) concentration of IAA. The root length of bglu10 and bglu24 did not respond to ABA, whereas that of bglu33 increased significantly in response to a high (0.05 µM) concentration of ABA. Quantitative real-time polymerase chain reaction (qRT-PCR) analysis showed that expression of Os4BGlu10 was up-regulated by polyethylene glycol (PEG), whereas that of Os6BGlu24 was up-regulated by 0.25 µM IAA, and Os9BGlu33 was up-regulated by PEG, IAA, and ABA. Taken together, we demonstrate that Os4BGlu10, Os6BGlu24, and Os9BGlu33 play specific roles in seed germination, root elongation, and drought tolerance with various relation with IAA and ABA signaling.


ABA Drought tolerant β-Glucosidase Rice Root elongation Seed germination 



ABA glucose ester




Days after imbibition


Variable fluorescence/maximal fluorescence


Polyethylene glycol


Relative water content



This work was supported by the Grants of the National Key Research and Development program of China (2016YFC0502304-03), and the National Natural Science Foundation of China (31571760), and the Creative Group Project of the Rice Industry Technological System of Tianjin (No. ITTRRS2018005), and the Key Program of the Natural Science Foundation of Tianjin (No. 17JCZDJC34000).

Supplementary material

425_2019_3125_MOESM1_ESM.doc (195 kb)
Supplementary material 1 (DOC 195 kb)


  1. Alarcón MV, Lloret PG, Salguero J (2014) The development of the maize root system: role of auxin and ethylene. In: Morte A, Varma A (eds) Root engineering. Springer, Berlin Heidelberg, pp 75–103CrossRefGoogle Scholar
  2. Aloni R (2013) Role of hormones in controlling vascular differentiation and the mechanism of lateral root initiation. Planta 238:819–830CrossRefGoogle Scholar
  3. Atkinson JA, Rasmussen A, Traini R, Voß U, Sturrock C, Mooney SJ, Wells DM, Bennett MJ (2014) Branching out in roots: uncovering form, function, and regulation. Plant Physiol 166:538–550CrossRefGoogle Scholar
  4. Baiya S, Hua Y, Ekkhara W, Ketudat Cairns JR (2014) Expression and enzymatic properties of rice (Oryza sativa L.) monolignol β-glucosidases. Plant Sci 227:101–109CrossRefGoogle Scholar
  5. Baiya S, Mahong B, Lee SK, Jeon JS, Ketudat Cairns JR (2018) Demonstration of monolignol β-glucosidase activity of rice Os4BGlu14, Os4BGlu16 and Os4BGlu18 in Arabidopsis thaliana bglu45 mutant. Plant Physiol Biochem 127:223–230CrossRefGoogle Scholar
  6. Bi L, Weng L, Jiang Z, Xiao H (2018) The tomato IQD gene SUN24 regulates seed germination through ABA signaling pathway. Planta 248:919–931CrossRefGoogle Scholar
  7. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171CrossRefGoogle Scholar
  8. Coutinho PM, Henrissat B (1999) Carbohydrate-active enzymes: an integrated database approach. In: Davies GJ, Gilbert HJ, Henrissat B, Svensson B (eds) Recent advances in carbohydrate engineering. Royal Society of Chemistry, Cambridge, UK, pp 3–11Google Scholar
  9. Dietz KJ, Sauter A, Wichert K, Messdaghi D, Hartung W (2000) Extracellular β-glucosidase activity in barley involved in the hydrolysis of ABA glucose conjugate in leaves. J Exp Bot 51:937–944CrossRefGoogle Scholar
  10. Escamilla-Treviño LL, Chen W, Card ML, Shih MC, Cheng CL, Poulton JE (2006) Arabidopsis thaliana beta-glucosidases BGlu45 and BGlu46 hydrolyse monolignol glucosides. Phytochemistry 67:1651–1660CrossRefGoogle Scholar
  11. Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45CrossRefGoogle Scholar
  12. Harris JM (2015) Abscisic acid: hidden architect of root system structure. Plants (Basel) 4:548–572CrossRefGoogle Scholar
  13. Hua Y, Ekkhara W, Sansenya S, Srisomsap C, Roytrakul S, Saburi W, Takeda R, Matsuura H, Mori H, Ketudat Cairns JR (2015) Identification of rice Os4BGlu13 as a β-glucosidase which hydrolyzes gibberellin A4 1-O-β-d-glucosyl ester, in addition to tuberonic acid glucoside and salicylic acid derivative glucosides. Arch Biochem Biophys 583:36–46CrossRefGoogle Scholar
  14. Huang Y, Sun MM, Ye Q, Wu XQ, Wu WH, Chen YF (2017) Abscisic acid modulates seed germination via ABA INSENSITIVE5-mediated PHOSPHATE1. Plant Physiol 175:1661–1668CrossRefGoogle Scholar
  15. Inukai Y, Sakamoto T, Ueguchi-Tanaka M, Shibata Y, Gomi K, Umemura I, Hasegawa Y, Ashikari M, Kitano H, Matsuoka M (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling. Plant Cell 17:1387–1396CrossRefGoogle Scholar
  16. Jakubowska A, Kawalczyk S (2005) A specific enzyme hydrolyzing 6-O (4-O)-indole-3-ylacetyl-β-d-glucose in immature kernels of Zea mays. J Plant Physiol 162:207–213CrossRefGoogle Scholar
  17. Ketudat Cairns JR, Esen A (2010) β-Glucosidases. Cell Mol Life Sci 67:3389–3405CrossRefGoogle Scholar
  18. Ketudat Cairns JR, Mahong B, Baiya S, Jeon JS (2015) β-Glucosidases: multitasking, moonlighting or simply misunderstood? Plant Sci 241:246–259CrossRefGoogle Scholar
  19. Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120CrossRefGoogle Scholar
  20. Léon-Kloosterziel KM, Gil MA, Ruijs GJ, Jacobsen SE, Olszewski NE, Schwartz SH, Zeevaart JA, Koornneef M (1996) Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J 10:655–661CrossRefGoogle Scholar
  21. Liu HY, Ren XQ, Zhu JZ, Wu X, Liang CJ (2018) Efect of exogenous abscisic acid on morphology, growth and nutrient uptake of rice (Oryza sativa) roots under simulated acid rain stress. Planta 248:647–659CrossRefGoogle Scholar
  22. Lombard V, Golaconda HR, Drula E, Coutinho PM, Henrissat B (2014) The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 42:D490–D495CrossRefGoogle Scholar
  23. Maia J, Dekkers BJW, Dolle MJ, Ligterink W, Hilhorst HWM (2014) Abscisic acid (ABA) sensitivity regulates desiccation tolerance in germinated Arabidopsis seeds. New Phytol 203:81–93CrossRefGoogle Scholar
  24. Opassiri R, Ketudat Cairns JR, Akiyama T, Wara-Aswapati O, Svasti J, Esen A (2003) Characterization of a rice β-glucosidase highly expressed in flower and germinating shoot. Plant Sci 165:627–638CrossRefGoogle Scholar
  25. Opassiri R, Hua Y, Wara-Aswapati O, Akiyama T, Svasti J, Esen A, Ketudat Cairns JR (2004) Beta-glucosidase, exo-beta-glucanase and pyridoxine transglucosylase activities of rice BGlu1. Biochem J 379:125–131CrossRefGoogle Scholar
  26. Opassiri R, Pomthong B, Onkoksoong T, Akiyama T, Esen A, Ketudat Cairns JR (2006) Analysis of rice glycosyl hydrolase family 1 and expression of Os4bglu12 beta-glucosidase. BMC Plant Biol 6:33CrossRefGoogle Scholar
  27. Sato H, Takasaki H, Takahashi F, Suzuki T, Iuchi S, Mitsuda N, Ohme-Takagi M, Ikeda M, Seo M, Yamaguchi-Shinozaki K, Shinozaki K (2018) Arabidopsis thaliana NGATHA1 transcription factor induces ABA biosynthesis by activating NCED3 gene during dehydration stress. Proc Natl Acad Sci USA 115:E11178–E11187CrossRefGoogle Scholar
  28. Seshadri S, Akiyama T, Opassiri R, Kuaprasert B, Cairns JK (2009) Structural and enzymatic characterization of Os3BGlu6, a rice beta-glucosidase hydrolyzing hydrophobic glycosides and (1 → 3)- and (1 → 2)-linked disaccharides. Plant Physiol 151:47–58CrossRefGoogle Scholar
  29. Shen JL, Li CL, Wang M, He LL, Lin MY, Chen DH, Zhang W (2017) Mitochondrial pyruvate carrier 1 mediates abscisic acid-regulated stomatal closure and the drought response by affecting cellular pyruvate content in Arabidopsis thaliana. BMC Plant Biol 17:217CrossRefGoogle Scholar
  30. Sherameti I, Venus Y, Drzewiecki C, Tripathi S, Dan VM, Nitz I, Varma A, Grundler FM, Oelmüller R (2008) PYK10, a beta-glucosidase located in the endoplasmatic reticulum, is crucial for the beneficial interaction between Arabidopsis thaliana and the endophytic fungus Piriformospora indica. Plant J 54:428–439CrossRefGoogle Scholar
  31. Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22:3560–3573CrossRefGoogle Scholar
  32. Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 9:e1003577CrossRefGoogle Scholar
  33. Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45CrossRefGoogle Scholar
  34. Wang PT, Liu H, Hua HJ, Wang L, Song CP (2011) A vacuole localized β-glucosidase contributes to drought tolerance in Arabidopsis. Chinese Sci Bull 56:3538–3546CrossRefGoogle Scholar
  35. Wolters H, Jürgens G (2009) Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet 10:305–317CrossRefGoogle Scholar
  36. Xiao HM, Cai WJ, Ye TT, Ding J, Feng YQ (2018) Spatio-temporal profiling of abscisic acid, indoleacetic acid and jasmonic acid in single rice seed during seed germination. Anal Chim Acta 1031:119–127CrossRefGoogle Scholar
  37. Xu Z, Escamilla-Treviño L, Zeng L, Lalgondar M, Bevan D, Winkel B, Mohamed A, Cheng CL, Shih MC, Poulton J, Esen A (2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol Biol 55:343–367CrossRefGoogle Scholar
  38. Yu L, Li Q, Zhu Y, Afzal MS, Li L (2018) An auxin-induced β-type endo-1,4-β-glucanase in poplar is involved in cell expansion and lateral root formation. Planta 24:1149–1161CrossRefGoogle Scholar
  39. Zhang H, Han W, De Smet I, Talboys P, Loya R, Hassan A, Rong H, Jürgens G, Knox JP, Wang MH (2010) ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis primary root meristem. Plant J 64:764–774CrossRefGoogle Scholar
  40. Zhang H, Zhu H, Pan Y, Yu Y, Luan S, Li L (2014) A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol Plant 7:1522–1532CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biochemistry and Molecular Biology, College of Life SciencesNankai UniversityTianjinChina
  2. 2.Department of Genetics and Cell Biology, College of Life SciencesNankai UniversityTianjinChina

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