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Acta Agronomica Sinica ›› 2022, Vol. 48 ›› Issue (12): 3029-3044.doi: 10.3724/SP.J.1006.2022.14237

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Genome-wide analysis of terpene synthase (TPS) gene family and its expression under biological stress in Saccharum spontaneum

LIN Huan-Tai(), ZHANG Tian-Jie, SHI Meng-Ting, GUO Yan-Fang, GAO San-Ji, WANG Jin-Da()   

  1. National Engineering Research Center for Sugarcane, Fujian Agriculture and Forestry University, Fuzhou 350002, Fujian, China
  • Received:2021-12-15 Accepted:2022-03-25 Online:2022-12-12 Published:2022-04-19
  • Contact: WANG Jin-Da E-mail:471250594@qq.com;jdwang@fafu.edu.cn
  • Supported by:
    National Key Research and Development Program of China(2018YFD201100);China Agricultural Systrm of MOF and MARA(Sugar, CARS-170302);Innovation Training Program for College Students of Fujian Province(S202110389051);Special Fund for Science and Technology Innovation of Fujian Agriculture and Forestry University(CXZX2020084A)

Abstract:

Terpenoids produced by the action of terpene synthase (TPS) enzymes play important roles in plant biotic and abiotic stress. Saccharum spontaneum, an important parent material of modern sugarcane cultivars, contains a large number of stress resistance genes. To investigate the characteristics and functions of the TPS gene family in S. spontaneum, 39 SsTPS genes were identified in S. spontaneum genome that encoded proteins with two conserved domains (PF01397 and PF03936) by using an HMMER search. The SsTPS proteins were divided into TPS-a, b, e/f, and g subfamilies. The SsTPS gene family had mainly expanded through segmental duplications, and a total of 12 SsTPS genes involved in segmental duplication events. In addition, qRT-PCR showed that the expression patterns of some SsTPS genes differed in S. spontaneum between Spodoptera frugiperda-stressed and Xanthomonas albilineans-infected plants, whereas the relative expression levels of seven SsTPS genes were strongly up-regulated. Notably, SsTPS15 were up-regulated in response to Spodoptera frugiperda-stressed but were down-regulated by X. albilineans infection, while SsTPS26, SsTPS37, and SsTPS39 had the opposite results. These results will be of great significance to further understanding the biological roles of terpene synthases and to develop resistant breeding in S. spontaneum.

Key words: Saccharum spontaneum, terpene synthase gene, biotic stresses, expression analysis, resistance breeding

Table 1

Primer sequence used to detect SsTPS gene expression level"

基因名称
Gene name
正向引物
Forward primer (5'-3')
反向引物
Reverse primer (5'-3')
SsTPS5 AGTACCGCATGCCCTACCTA CACCGCTTCTTGCTGAAACC
SsTPS6 AGTACCGCATGCCCTACCTA CGCTGCAAGTGTTCCTCAAC
SsTPS8 ATGATGTTCAGGGGCTGCAA CATGTATGCACGCTTGGGTG
SsTPS10 AGGGGAAAGTGCGTCAGATG AGTGTGGATACGGCTTAGCG
SsTPS15 AAAAGACCGGACCTTCCACC CATGTATGCACGCTTGGGTG
SsTPS18 ACCAAGGAGGCATTCGAGTG CGCGTTCTTCCTCCCTTTCT
SsTPS26 GTCCCATGCACTCCATCACA GAGGTGGCAACGGTTCCTAA
SsTPS27 AATGGGCTCTCACCTTTCCG AAGCTTGTTCACGCTCATGC
SsTPS35 TGTTCCTAGGCCATGCAAGG TTTTGGACTCCGAGTGGCTC
SsTPS36 TGCTGCTGCGCAATGATTTT GGTCGCTCTTCTGACGTTGA
SsTPS37 GAGCCAAGCCTTGCAGAGTA ATGGGCAGGCTCTGTAGGTA
SsTPS39 GAAATACCTGTGGTGCGGGA CCACAACATAGACAAGCGCG
GAPDH CACGGCCACTGGAAGCA TCCTCAGGGTTCCTGATGCC

Table 2

Basin information and physiochemical properties of SsTPS genes family in S. spontaneum"

基因名称
Gene name
基因编号
Gene ID
氨基酸数
Number of amino acids
等电点
pI
分子量
Molecular weight (kD)
负电荷残基
Asp+Glu
正电荷残基Arg+Lys 不稳定系数Coefficient of instability 平均疏水性 GRAVY 脂肪系数 AI α-螺旋
α-helix(%)
延伸链
Extended chain (%)
无规则卷曲
Random curl (%)
SsTPS1 Sspon.01G0009730-1A 514 5.90 59,392.66 72 62 36.28 -0.306 88.29 57.39 11.67 30.93
SsTPS2 Sspon.01G0010010-1A 496 5.29 57,214.41 78 57 37.65 -0.288 94.92 54.03 14.72 31.25
SsTPS3 Sspon.01G0044880-1B 497 5.75 56,761.45 69 54 40.04 -0.312 83.84 49.90 17.51 32.60
SsTPS4 Sspon.04G0011840-1A 735 9.77 81,962.81 74 104 60.66 -0.460 75.17 43.67 8.03 48.30
SsTPS5 Sspon.04G0011840-2B 353 5.78 41,253.51 51 43 47.03 -0.333 87.00 64.31 3.68 32.01
SsTPS6 Sspon.04G0011840-3C 501 6.43 57,711.12 62 58 45.18 -0.311 87.96 55.09 6.99 37.92
SsTPS7 Sspon.05G0015000-1A 581 5.53 66,604.19 78 61 39.07 -0.216 91.02 51.29 12.22 36.49
SsTPS8 Sspon.06G0010490-1P 528 5.33 61,308.56 76 59 39.80 -0.173 98.26 52.65 12.12 35.23
SsTPS9 Sspon.06G0010500-1A 376 5.10 43,465.54 59 41 52.71 -0.328 87.95 52.39 11.17 36.44
SsTPS10 Sspon.06G0011520-1A 433 5.84 49,561.84 62 51 40.69 -0.242 83.44 55.43 9.70 34.87
SsTPS11 Sspon.06G0011680-1A 468 5.32 53,911.93 71 58 49.94 -0.247 97.67 60.47 7.69 31.84
SsTPS12 Sspon.06G0010490-1A 538 5.34 62,470.81 78 61 40.28 -0.201 96.43 50.74 12.64 36.62
SsTPS13 Sspon.06G0021690-1B 325 5.52 37,701.75 51 39 46.74 -0.380 89.14 55.38 12.62 32.00
SsTPS14 Sspon.06G0023410-1B 397 5.47 46,236.32 64 52 38.72 -0.254 96.93 50.13 12.85 37.03
SsTPS15 Sspon.06G0010490-2B 538 5.34 62,468.83 78 61 40.74 -0.192 97.16 50.93 12.64 36.43
SsTPS16 Sspon.06G0011680-2B 607 5.96 70,631.16 81 70 49.39 -0.222 94.23 50.74 13.67 35.58
SsTPS17 Sspon.06G0024130-1B 606 5.97 70,317.44 86 74 53.41 -0.363 83.83 55.61 13.53 30.86
SsTPS18 Sspon.06G0015570-2B 533 5.29 61,439.38 76 57 45.23 -0.220 83.49 50.66 14.82 34.52
SsTPS19 Sspon.06G0023520-2C 491 5.08 57,333.63 76 54 49.64 -0.302 84.83 46.84 13.65 39.51
SsTPS20 Sspon.06G0011660-2C 482 5.04 55,885.74 75 53 48.91 -0.274 86.72 47.51 18.67 33.82
SsTPS21 Sspon.06G0011680-1P 414 5.47 47,542.37 62 48 48.39 -0.301 93.16 53.86 10.63 35.51
SsTPS22 Sspon.06G0030650-1C 358 9.40 41,189.25 38 51 38.63 -0.391 79.55 46.37 13.69 39.94
SsTPS23 Sspon.06G0011680-3C 468 5.15 53,761.70 72 55 51.78 -0.219 98.93 58.55 9.83 31.62
SsTPS24 Sspon.06G0034360-1D 317 4.93 36,898.43 50 32 39.19 -0.134 91.29 48.26 17.98 33.75
SsTPS25 Sspon.06G0011680-2P 333 8.65 38,083.58 38 42 35.22 -0.328 83.75 38.44 21.32 40.24
SsTPS26 Sspon.06G0024130-2D 545 5.56 63,780.15 81 68 48.69 -0.286 90.11 53.39 13.58 33.03
SsTPS27 Sspon.06G0024130-1P 497 5.71 57,610.39 75 65 43.03 -0.181 93.00 51.71 17.30 30.99
SsTPS28 Sspon.06G0011680-4D 328 8.47 37,598.00 37 40 33.44 -0.324 82.65 42.38 17.38 40.24
SsTPS29 Sspon.07G0027750-1B 509 5.55 59,706.37 75 59 55.08 -0.414 90.84 52.65 9.23 38.11
SsTPS30 Sspon.08G0029890-1D 629 5.83 71,361.82 80 67 49.40 -0.160 86.38 46.26 13.67 40.06
SsTPS31 Sspon.01G0039100-1B 348 5.62 39,581.24 49 39 48.50 -0.288 84.74 47.14 12.93 39.66
SsTPS32 Sspon.01G0039100-2C 550 8.25 62,827.75 67 70 54.38 -0.376 82.91 50.36 9.45 40.18
SsTPS33 Sspon.04G0000830-1A 388 5.42 44,015.32 47 38 54.09 -0.088 93.84 55.41 7.47 37.11
SsTPS34 Sspon.05G0030980-1C 545 6.04 62,692.00 73 67 49.04 -0.309 84.02 41.47 12.29 46.24
SsTPS35 Sspon.05G0002480-3D 783 6.03 87,936.45 90 18 46.73 -0.168 89.13 47.51 11.11 41.38
SsTPS36 Sspon.04G0020000-1A 550 5.33 62,580.79 74 53 52.94 -0.116 92.62 49.27 16.55 34.18
SsTPS37 Sspon.04G0019960-2C 515 5.28 59,084.06 71 52 47.41 -0.090 96.37 53.59 14.17 32.23
SsTPS38 Sspon.04G0020000-4P 563 6.13 63,167.56 68 58 50.45 -0.145 89.68 52.75 11.90 35.35
SsTPS39 Sspon.04G0020000-3D 552 5.25 63,021.29 78 56 51.02 -0.123 95.27 54.53 11.78 33.70

Fig. 1

Phylogenetic tree of TPS gene family in S. spontaneum (Ss), Oryza sativa (Os), and Sorghum bicolor (Sb) TPS-a, b, e/f, and g represent different branches of TPS gene family, respectively."

Fig. 2

Genetic structures of gene family members of S. spontaneum A: the phylogenetic tree of SsTPSs. B: the prediction of intron-exon structure of SsTPSs. C: the motifs prediction of SsTPSs. D: the motif of base sequence structure."

Fig. 3

Chromosomal localization of the terpene synthase genes family in S. spontaneum"

Fig. 4

Collinear analysis of the terpene synthase genes family in S. spontaneum"

Fig. 5

Types and numbers of cis-acting elements in promoter regions of each member of the TPS gene family in S. spontaneum 1-39 represent the S. spontaneum TPS gene family member from SsTPS1 to SsTPS39, respectively."

Fig. 6

Heat map of the expression of TPS genes in different tissues of S. spontaneum"

Fig. 7

Relative expression levels of 12 candidate SsTPS genes in S. spontaneum under S. frugiperda stress *, **, and *** mean significant difference at the 0.05, 0.01, and 0.001 probability levels, respectively."

Fig. 8

Expression analysis of 12 SsTPS genes under X. albilineans infection in S. spontaneum Different lowercase letters above the bars mean significant difference at the 0.05 probability level among the treatments."

[1] Tholl D. Biosynthesis and biological functions of terpenoids in plants. Adv Biochem Eng Biotechnol, 2015, 148: 63-106.
[2] 韩娟娟, 李喜旺, 刘丰静, 辛肇军, 张瑾, 张新, 孙晓玲. 茶丽纹象甲对茶树品种的取食选择及其诱导的4种萜烯类化合物. 茶叶科学, 2017, 37: 220-227.
Han J J, Li X W, Liu F J, Xin Z J, Zhang J, Zhang X, Sun X L. Feeding selection of tea cultivars by the tea weevil and the four induced terpenoids. J Tea Sci, 2017, 37: 220-227. (in Chinese with English abstract)
[3] Hunsigi G, Yekkeli N R, Perumal L, Thippannavar M B. Antibiosis in sugarcane genotypes against woolly aphid Ceratavacuna lanigera Zehntner. Curr Sci India, 2006, 90: 771-772.
[4] 赵善欢, 曹毅, 彭中健, 黄家总. 应用天然植物产品川楝素防治菜青虫试验. 植物保护学报, 1985, 12: 125-132.
Zhao S H, Cao Y, Peng Z J, Huang J Z. Experiments on the control of Pieris rapae with Toosendanin. J Plant Prot, 1985, 12: 125-132. (in Chinese)
[5] Irmisch S, Jiang Y, Chen F, Gershenzon J, Köllner T G. Terpene synthases and their contribution to herbivore-induced volatile emission in western balsam poplar (Populus trichocarpa). BMC Plant Biol, 2014, 14: 270.
doi: 10.1186/s12870-014-0270-y pmid: 25303804
[6] De Moraes C M, Mescher M C, Tumlinson J H. Caterpillar- induced nocturnal plant volatiles repel conspecific females. Nature, 2001, 410: 577-580.
doi: 10.1038/35069058
[7] Cheniclet C. Effects of wounding and fungus inoculation on terpene producing systems of maritime pine. J Exp Bot, 1987, 38: 1557-1572.
doi: 10.1093/jxb/38.9.1557
[8] 孟雪, 王志英, 吕慧. 绿萝和常春藤主要挥发性成分及其对5种真菌的抑制活性. 园艺学报. 2010, 37: 971-976.
Meng X, Wang Z Y, Lyu H. The volatile constituents analysis of Scindapsus aureum and Hedera nepalensis var. sinensis and their inhibition against five fungi. Acta Hortic Sin, 2010, 37: 971-976. (in Chinese with English abstract)
[9] Cui J, Liang J. Research progress of antibacterial effects of citrus peel essential oils. Sci Technol Cereals, 2018, 26: 35-39.
[10] Lu K, Li X, Zhou J, Xie X, Qi S, Zhou Q. Influence of the herbivore-induced rice volatiles on fungal disease. Chin Sci Bull, 2010, 55: 47-52.
[11] Liu F, Zuo Z J, Xu G P, Wu X B, Zheng J, Gao R F, Zhang R M, Gao Y. Physiological responses to drought stress and the emission of induced volatile organic compounds in Rosmarinus officinalis. J Plant Ecol, 2013, 37: 454-463.
[12] Blanch J S, Peñuelas J, Llusià J. Sensitivity of terpene emissions to drought and fertilization in terpene-storing Pinus halepensis and non-storing Quercus ilex. Physiol Plant, 2007, 131: 211-225.
[13] Kainulainen P, Oksanen J, Palomäki V, Holopainen J K, Holopainen T. Effect of drought and waterlogging stress on needle monoterpenes of Picea abies. Can J Bot, 1992, 70: 1613-1616.
doi: 10.1139/b92-203
[14] Finn R D, Coggill P, Eberhardt R Y, Eddy S R, Mistry J, Mitchell A L, Potter S C, Punta M, Quewshi M, Sangrador-Vegas A, Salazar G A, John Tate S, Bereman A. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res, 2015, 44: D279-D285.
[15] Starks C M, Back K, Chappell J, Novel J P. Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase. Science, 1997, 277: 1815-1820.
pmid: 9295271
[16] Falara V, Akhtar T A, Nguyen T H, Spyropoulou E A, Bleeker P M, Schauvinhold I, Matsuba Y, Bonini M E, Schilmiller A L, Last R L. The tomato terpene synthase gene family. Plant Physiol, 2011, 157: 770-789.
doi: 10.1104/pp.111.179648 pmid: 21813655
[17] Jiang S Y, Jin J, Sarojam R, Ramachandran S. A comprehensive survey on the terpene synthase gene family provides new insight into its evolutionary patterns. Genome Biol Evol, 2019, 11: 2078-2098.
doi: 10.1093/gbe/evz142
[18] Chen F, Tholl D, Bohlmann J R, Pichersky E. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J, 2011, 66: 212-229.
doi: 10.1111/j.1365-313X.2011.04520.x
[19] Nieuwenhuizen N J, Green S A, Chen X, Bailleul E J D, Matich A J, Wang M Y, Atkinson R G. Functional genomics reveals that a compact terpene synthase gene family can account for terpene volatile production in apple. Plant Physiol, 2013, 161: 787-804.
doi: 10.1104/pp.112.208249 pmid: 23256150
[20] Tuskan G A, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science, 2006, 313: 1596-1604.
pmid: 16973872
[21] Li G, Koellner T G, Yin Y, Jiang Y, Chen H, Xu Y, Gershenzon J, Pichersky E, Chen F. Nonseed plant Selaginella moellendorfii has both seed plant and microbial types of terpene synthases. Proc Natl Acad Sci USA, 2012, 109: 14711-14715.
doi: 10.1073/pnas.1204300109
[22] Bohlmann J, Meyer-Gauen G, Croteau R. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA, 1998, 95: 4126-4133.
doi: 10.1073/pnas.95.8.4126
[23] Degenhardt J, Kllner T G, Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry, 2009, 70: 1621-1637.
doi: 10.1016/j.phytochem.2009.07.030 pmid: 19793600
[24] Külheim C, Padovan A, Hefer C, Krause S T, Köllner T G, Myburg A A, Degenhardt J, Foley W J. The eucalyptus terpene synthase gene family. BMC Genomics, 2015, 16: 450.
doi: 10.1186/s12864-015-1598-x pmid: 26062733
[25] Whittington D A, Wise M L, Urbansky M, Coates R M, Croteau R B, Christianson D W. Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase. Proc Natl Acad Sci USA, 2002, 99: 15375-15380.
doi: 10.1073/pnas.232591099
[26] Christianson D W. Structural and chemical biology of terpenoid cyclases. Chem Rev, 2017, 117: 11570-11648.
doi: 10.1021/acs.chemrev.7b00287 pmid: 28841019
[27] Ali A, Khan M, Sharif R, Mujtaba M, Gao S J. Sugarcane omics: an update on the current status of research and crop improvement. Plants (Basel), 2019, 8: 344.
[28] Diniz A L, Ferreira S S, Ten-Caten F, Margarido G R A, Santos J M, S Barbosa G V, Carneiro M S, Souza G M. Genomic resources for energy cane breeding in the post genomics era. Comput Struct Biotechnol, 2019, 17: 1404-1414.
[29] Olivier G, Gaetan D, Rudie A, Jane G, Bernard P, Karen A, Jerry J, Guillaume M, Carine C, Catherine H. A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nat Commun, 2018, 9: 2638.
doi: 10.1038/s41467-018-05051-5 pmid: 29980662
[30] Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X, Zhu F, Jones T, Zhu X, Bowers J, Wai C, Zheng C, Shi Y, Chen S, Xu X, Yue J, Nelson D, Huang L, Li Z, Ming R. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet, 2018, 50: 1565-1573.
doi: 10.1038/s41588-018-0237-2
[31] Xu F, He L, Gao S, Su Y C, Li F, Xu L. Comparative analysis of two sugarcane ancestors Saccharum officinarum and S. spontaneum based on complete chloroplast genome sequences and photosynthetic ability in cold stress. Int J Mol Sci, 2019, 20: 3828.
doi: 10.3390/ijms20153828
[32] Souza G, Van Sluys M A, Lembke C G, Lee H, Margarido G R A, Hotta C, Gaiarsa J, Lima Diniz A, Oliveira M M, Ferreira S S, Nishiyama Jr M Y, Caten F, Ragagnin G T, Andrade P M, De Souza R F, Nicastro G, Pandya R, Kim C, Guo H, Durham A M, Carnerio M S, Zhang J S, Zhang X T, Zhang Q, Ming R, Schatz M C, Davidson B, Paterson M C, Heckerman D. Assembly of the 373k gene space of the polyploid sugarcane genome reveals reservoirs of functional diversity in the world's leading biomass crop. Gigascience, 2019, 8: giz129.
doi: 10.1093/gigascience/giz129
[33] Royer M, Pieretti I, Cociancich S, Rott P. Recent progress in understanding three major bacterial diseases of sugarcane: gumming, leaf scald and ratoon stunting. Burleigh Dodds, 2018, 26: 311-336.
[34] 李傲梅, 谭宏伟, 魏吉利, 商显坤, 黄东亮, 何为中. 草地贪夜蛾在甘蔗上的发生及防治措施. 植物保护学报, 2020, 47: 735-739.
Li A M, Tan H W, Wei J L, Shang X K, Huang D L, He W Z. Advances in outbreak and control of fall armyworm Spodoptera frugiperda on sugarcane. J Plant Prot, 2020, 47: 735-739. (in Chinese with English abstract)
[35] Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13: 1194-1202.
doi: S1674-2052(20)30187-8 pmid: 32585190
[36] Wang D, Tang H, Debarry J D, Tan X, Li J P, Wang X Y, Lee T H, Jin H Z, Marler B, Guo H, Kissinger J C, Paterson A H. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res, 2010, 40: e49.
doi: 10.1093/nar/gkr1293
[37] Lin L H, Ntambo M S, Rott P C, Wang Q N, Lin Y H, Fu H Y, Gao S J. Molecular detection and prevalence of Xanthomonas albilineans, the causal agent of sugarcane leaf scald, in China. Crop Prot, 2018, 109: 17-23.
doi: 10.1016/j.cropro.2018.02.027
[38] Livak K J, Schmittgen T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 2001, 25: 402-408.
doi: 10.1006/meth.2001.1262 pmid: 11846609
[39] Dudareva N, Cseke L, Blanc V M, Pichersky E. Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell, 1996, 8: 1137-1148.
pmid: 8768373
[40] Cannon S B, Mitra A, Baumgarten A, Young N D, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol, 2004, 4: 10.
doi: 10.1186/1471-2229-4-10
[41] Olsen J L, Rouze P, Verhelst B, Lin Y C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Topel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Bostrom C, Chovatia M, Grimwood J, Jenkins J W, Jueterbock A, Mraz A, Stam W T, Tice H, Bornberg-Bauer E, Green P J, Pearson G A, Procaccini G, Duarte C M, Schmutz J, Reusch T B, Van de Peer Y. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature, 2016, 530: 331-335.
doi: 10.1038/nature16548
[42] Jiao Y, Liu X, Jiang H, Chen R. Research advances of plant tissue specific promoters. J Agric Sci Technol (Iran), 2019, 21: 18-28.
[43] Aubourg S, Lecharny A, Bohlmann J. Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genomics, 2002, 267: 730-745.
pmid: 12207221
[44] Martin D M, Aubourg S, Schouwey M B, Daviet L, Schalk M, Toub O, Lund S T, Bohlmann J. Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, flcdna cloning, and enzyme assays. BMC Plant Biol, 2012, 10: 226.
doi: 10.1186/1471-2229-10-226
[45] Kumar Y, Khan F, Rastogi S. Genome-wide detection of terpene synthase genes in holy basil (Ocimum sanctum L.). PLoS One, 2018, 13: e0207097.
[46] Liu J Y, Huang F, Wang X. Genome-wide analysis of terpene synthases in soybean: functional characterization of GmTPS3. Gene, 2014, 544: 83-92.
doi: 10.1016/j.gene.2014.04.046
[47] Chen X, Yang W, Zhang L Q. Genome-wide identification, functional and evolutionary analysis of terpene synthases in pineapple. Comp Biol Chem, 2017, 70: 40-48.
doi: 10.1016/j.compbiolchem.2017.05.010
[48] Xiong W D, Wu P Z, Jia Y X. Genome-wide analysis of the terpene synthase gene family in physic nut (Jatropha curcas L.) and functional identification of six terpene synthases. Tree Genet Genom, 2016, 12: 97.
doi: 10.1007/s11295-016-1054-3
[49] Martin H. Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol, 2014, 204: 297-306.
doi: 10.1111/nph.12977
[50] Jiang Z, Jacob J A, Loganathachetti D S. β-elemene: mechanistic studies on cancer cell interaction and its chemosensitization effect. Front Pharmacol, 2017, 8: 105.
doi: 10.3389/fphar.2017.00105 pmid: 28337141
[51] Paddon C J, Keasling J D. Semi-synthetic artemisinin: a model for the use of synthetic biology in pharmaceutical development. Nat Rev Microbiol, 2014, 12: 355-367.
doi: 10.1038/nrmicro3240 pmid: 24686413
[52] Cheng A X, Xiang C Y, Li J X. The rice (E)-beta-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry, 2007, 68: 1632-1641.
doi: 10.1016/j.phytochem.2007.04.008
[53] Xiao Y, Wang Q, Erb M. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol Lett, 2012, 15: 1130-1139.
doi: 10.1111/j.1461-0248.2012.01835.x pmid: 22804824
[54] Chen X, Chen H, Yuan J S, Köllner T G, Chen Y, Guo Y, Zhuang X, Chen X, Zhang Y, Fu J, Nebenführ A, Guo Z, Chen F. The rice terpene synthase gene OsTPS19 functions as an (S)-limonene synthase in planta and its overexpression leads to enhanced resistance to the blast fungus Magnaporthe oryzae. Plant Biotechnol J, 2018, 16: 1778-1787.
doi: 10.1111/pbi.12914
[55] Rodríguez A, Andrés V S, Cervera M, Redondo A, Leandro P. The monoterpene limonene in orange peels attracts pests and microorganisms. Plant Signal Behav, 2011, 6: 1820-1823.
doi: 10.4161/psb.6.11.16980 pmid: 22212123
[56] Huang M, Sanchez-Moreiras A M, Abel C. Sohrabi R, Lee S, Gershenzon J, Tholl D. The major volatile organic compound emitted from Arabidopsis thaliana flowers, the sesquiterpene (E)-β-caryophyllene, is a defense against a bacterial pathogen. New Phytol, 2012, 193: 997-1008.
doi: 10.1111/j.1469-8137.2011.04001.x
[57] Chiriboga M X, Campos-Herrera R, Jaffuel G, RóDer G, Turlings T C J. Diffusion of the maize root signal (E)-β-caryophyllene in soils of different textures and the effects on the migration of the entomopathogenic nematode Heterorhabditis megidis. Rhizosphere, 2017, 3: 53-59.
doi: 10.1016/j.rhisph.2016.12.006
[58] Ding Y, Huffaker A, KöLlner T G, Weckwerth P, Robert C A M, Spencer J L, Lipka A E, Schmelz E A. Selinene volatiles are essential precursors for maize defense promoting fungal pathogen resistance. Plant Physiol, 2017, 175: 1455-1468.
doi: 10.1104/pp.17.00879 pmid: 28931629
[59] 卢凯, 李欣, 周嘉良, 解晓军, 戚舒, 周强. 虫害诱导的水稻挥发物抑制水稻病原菌的生长. 科学通报, 2010, 55: 2927-2932.
Lu K, Li X, Zhou J L, Xie X J, Qi S, Zhou Q. Insect-induced rice volatiles inhibit the growth of rice pathogenic bacteria. Sci Bull, 2010, 55: 2927-2932. (in Chinese with English abstract)
[60] 刘小香, 陈秋波, 王真辉, 谢龙莲, 徐志. 巨尾桉挥发油对真菌和昆虫的化感作用. 生态学杂志, 2007, 26: 835-839.
Liu X X, Chen Q B, Wang Z H, Xie L L, Xu Z. Allelopathy of volatile oil from Eucalyptus grandis on fungi and insects. Chin J Ecol, 2007, 26: 835-839. (in Chinese with English abstract)
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