Multiple Roles of Berberine Bridge Enzyme Gene HbBBE1 in Response to Stress in Hevea brasiliensis Muell. Arg.

doi:10.7525/j.issn.1673-5102.2018.05.010

Abstract

Abstract: Berberine bridge enzyme(BBE,EC1.5.3.9) is a key enzyme in berberine biosynthesis. In this study, HbBBE1 gene was cloned in rubber tree by RT-PCR. The HbBBE1 promoter contained light, gibberellin, salicylic acid, wounding, fungal elicitor, defense, and stress responsive elements. The predicted protein of HbBBE1 contains a signal peptide, a trans membrane region, an FAD binding domain, and a BBE domain which is found specifically in the berberine bridge enzymes and berberine bridge-like enzymes. It shared the highest similarity with BBE protein from Manihot esculenta with 80.1% identical residues. Comparing expression among different tissues of rubber tree demonstrated that HbBBE1 has a particularly high expression level in the latex. HbBBE1 expression was significantly upregulated by biotic and abiotic stress, i.e. powdery mildew infection, drought stress, high intensity light irradiation, H₂O₂, and both tapping treatment in virgin trees and mechanical wounding in seedlings. Furthermore, HbBBE1 transcript was remarkably induced by application of exogenous hormones, including gibberellic acid(GA₃), salicylic acid(SA), ethephon(ET), methyl jasmonate(MeJA), and abscisic acid(ABA). Among these treatments, HbBBE1 transcript was quickly induced by GA₃ stimulation, and reached a maximum(6.3-fold) at 0.5 h. The increased expression of HbBBE1 was highly induced by ABA, ET, and H₂O₂ stimuli, and it accumulated dozens of times comparing that at the untreated control.To summarize, our study suggested that HbBBE1 played multiple roles in response to biotic and abiotic stress in rubber tree.

Key words: Hevea brasiliensis, berberine bridge enzyme, HbBBE1, stress response

CLC Number:

S794.1

WANG Meng, ZHNG Dong, LU Yan-Xi, XIAO Hua-Xing, ZHENG Fu-Cong, ZHANG Yu. Multiple Roles of Berberine Bridge Enzyme Gene HbBBE1 in Response to Stress in Hevea brasiliensis Muell. Arg.[J]. Bulletin of Botanical Research, 2018, 38(5): 704-713.

References

1. Dittrich H,Kutchan T M. Molecular cloning,expression,and induction of berberine bridge enzyme,an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack[J]. Proceedings of the National Academy of Sciences of the United States of America,1991,88(22):9969-9973.
2. Gaweska H M,Roberts K M,Fitzpatrick P F. Isotope effects suggest a stepwise mechanism for berberine bridge enzyme[J]. Biochemistry,2012,51(37):7342-7347.
3. Dzink J L,Socransky S S. Comparative in vitro activity of sanguinarine against oral microbial isolates[J]. Antimicrobial Agents and Chemotherapy,1985,27(4):663-665.
4. Cline S D,Coscia C J. Stimulation of sanguinarine production by combined fungal elicitation and hormonal deprivation in cell suspension cultures of Papaver bracteatum[J]. Plant Physiology,1988,86(1):161-165.
5. Schumacher H M,Gundlach H,Fiedler F,et al. Elicitation of benzophenanthridine alkaloid synthesis in Eschscholtzia cell cultures[J]. Plant Cell Reports,1987,6(6):410-413.
6. Eilert U,Kurz W G W,Constabel F. Stimulation of sanguinarine accumulation in Papaver somniferum cell cultures by fungal elicitors[J]. Journal of Plant Physiology,1985,119(1):65-76.
7. Facchini P J,Penzes C,Johnson A G,et al. Molecular characterization of berberine bridge enzyme genes from opium poppy[J]. Plant Physiology,1996,112(4):1669-1677.
8. Backhaus R A. Rubber formation in plants-a mini-review[J]. Israel Journal of Botany,1985,34(2-4):283-293.
9. Tang C R,Yang M,Fang Y F,et al. The rubber tree genome reveals new insights into rubber production and species adaptation[J]. Nature Plants,2016,2(6):16073.
10. Ayutthaya S I N,Do F C. Rubber trees affected by necrotic tapping panel dryness exhibit poor transpiration regulation under atmospheric drought[J]. Advanced Materials Research,2014,844:3-6.
11. Thomas M,Sumesh K V,Sreelatha S,et al. Biochemical evaluation of RRⅡ 400 series clones of Hevea brasiliensis for drought tolerance[J]. Indian Journal of Agricultural Biochemistry,2014,27(1):35-39.
12. Coupe M,Chrestin H. The hormonal stimulation of latex yield:physico-chemical and biochemical mechanisms of hormonal(ethylene) stimulation[M].//D'auzac J,Jacob J L,Chrestin H. Physiology of Rubber Tree Latex. Boca Raton,FL:CRC Press,1989:295-319.
13. Pujade-Renaud V,Clement A,Perrot-Rechenmann C,et al. Ethylene-induced increase in glutamine synthetase activity and mRNA levels in Hevea brasiliensis latex cells[J]. Plant Physiology,1994,105(1):127-132.
14. Liu J P,Zhuang Y F,Guo X L,et al. Molecular mechanism of ethylene stimulation of latex yield in rubber tree(Hevea brasiliensis) revealed by de novo sequencing and transcriptome analysis[J]. BMC Genomics,2016,17:257.
15. Wang L F,Wang M,Zhang Y. Effects of powdery mildew infection on chloroplast and mitochondrial functions in rubber tree[J]. Tropical Plant Pathology,2014,39(3):242-250.
16. Lee G I,Howe G A. The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression[J]. The Plant Journal,2003,33(3):567-576.
17. Wang L F. Physiological and molecular responses to drought stress in rubber tree(Hevea brasiliensis Muell. Arg.)[J]. Plant Physiology and Biochemistry,2014,83:243-249.
18. Wang L F. Physiological and molecular responses to variation of light intensity in rubber Tree(Hevea brasiliensis Muell. Arg.)[J]. PLoS One,2014,9(2):e89514.
19. Qin B,Zheng F C,Zhang Y. Molecular cloning and characterization of a Mlo gene in rubber tree(Hevea brasiliensis)[J]. Journal of Plant Physiology,2015,175:78-85.
20. Schmittgen T D,Livak K J. Analyzing real-time PCR data by the comparative C(T) method[J]. Nature Protocols,2008,3(6):1101-1108.
21. Hauschild K,Pauli H H,Kutchan T M. Isolation and analysis of a gene bbe1 encoding the berberine bridge enzyme from the California poppy Eschscholzia californica[J]. Plant Molecular Biology,1998,36(3):473-478.
22. Minami H,Kim J S,Ikezawa N,et al. Microbial production of plant benzylisoquinoline alkaloids[J]. Proceedings of the National Academy of Sciences of the United States of America,2008,105(21):7393-7398.
23. Broekaert W,Lee H I,Kush A,et al. Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree(Hevea brasiliensis)[J]. Proceedings of the National Academy of Sciences of the United States of America,1990,87(19):7633-7637.
24. Chye M L,Cheung K Y. β-1,3-Glucanase is highly-expressed in laticifers of Hevea brasiliensis[J]. Plant Molecular Biology,1995,29(2):397-402.
25. Long X Y,He B,Fang Y J,et al. Identification and characterization of the Glucose-6-Phosphate dehydrogenase gene family in the para rubber tree,Hevea brasiliensis[J]. Frontiers in Plant Science,2016,7:215.
26. Alam B,Nair D B,Jacob J. Low temperature stress modifies the photochemical efficiency of a tropical tree species Hevea brasiliensis:effects of varying concentration of CO₂ and photon flux density[J]. Photosynthetica,2005,43(2):247-252.
27. Li X,Bi Z H,Di R,et al. Identification of powdery mildew responsive genes in Hevea brasiliensis through mRNA differential display[J]. International Journal of Molecular Sciences,2016,17(2):181.
28. Bokma E,Van Koningsvelda G A,Jeronimus-Stratinghb M,et al. Hevamine,a chitinase from the rubber tree Hevea brasiliensis,cleaves peptidoglycan between the C-1 of N-acetylglucosamine and C-4 of N-acetylmuramic acid and therefore is not a lysozyme[J]. FEBS Letters,1997,411(2-3):161-163.
29. Bokma E,Barends T,Van Scheltinga A C T,et al. Enzyme kinetics of hevamine,a chitinase from the rubber tree Hevea brasiliensis[J]. FEBS Letters,2000,478(1-2):119-122.
30. Chow K S,Wan W L,Isa M N M,et al. Insights into rubber biosynthesis from transcriptome analysis of Hevea brasiliensis latex[J]. Journal of Experimental Botany,2007,58(10):2429-2440.
31. Wang X C,Shi M J,Wang D,et al. Comparative proteomics of primary and secondary lutoids reveals that chitinase and glucanase play a crucial combined role in rubber particle aggregation in Hevea brasiliensis[J]. Journal of Proteome Research,2013,12(11):5146-5159.
32. Bari R,Jones J D. Role of plant hormones in plant defence responses[J]. Plant Molecular Biology,2009,69(4):473-488.
33. Nakashima K,Yamaguchi-Shinozaki K. ABA signaling in stress-response and seed development[J]. Plant Cell Reports,2013,32(7):959-970.
34. Kajikawa M,Shoji T,Kato A,et al. Vacuole-localized berberine bridge enzyme-like proteins are required for a late step of nicotine biosynthesis in tobacco[J]. Plant Physiology,2011,155(4):2010-2022.
35. Kutchan T M,Dittrich H. Characterization and mechanism of the berberine bridge enzyme,a covalently flavinylated oxidase of benzophenanthridine alkaloid biosynthesis in plants[J]. Journal of Biological Chemistry,1995,270(41):24475-24481.
36. Daniel B,Pavkov-Keller T,Steiner B,et al. Oxidation of monolignols by members of the berberine bridge enzyme family suggests a role in plant cell wall metabolism[J]. Journal of Biological Chemistry,2015,290(30):18770-18781.

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