专题论坛

植物次生代谢产物生物合成基因簇研究进展

  • 朱璐 ,
  • 袁冲 ,
  • 刘义飞
展开
  • 湖北中医药大学, 武汉 430074

收稿日期: 2022-10-03

  录用日期: 2023-04-18

  网络出版日期: 2023-04-25

基金资助

国家自然科学基金(32270231);湖北省杰出青年基金(2019CFA097)

Research Progress on Plant Secondary Metabolite Biosyn-thetic Gene Clusters

  • Lu Zhu ,
  • Chong Yuan ,
  • Yifei Liu
Expand
  • Hubei University of Chinese Medicine, Wuhan 430074, China

Received date: 2022-10-03

  Accepted date: 2023-04-18

  Online published: 2023-04-25

摘要

植物产生的次生代谢产物为人类提供了丰富的药物、香料和工业原料。随着分子生物学和基因组学研究的快速发展, 目前已解析了多种植物的次生代谢产物生物合成基因簇(BGCs)。这为我们快速获取目标产物的生物合成通路和发掘新颖的天然产物开辟了新路径。该文重点围绕植物次生代谢产物生物合成基因簇的定义和特点、基本结构模型与演化以及调控机制等进行综述, 以期为相关研究提供理论依据和借鉴。

本文引用格式

朱璐 , 袁冲 , 刘义飞 . 植物次生代谢产物生物合成基因簇研究进展[J]. 植物学报, 2024 , 59(1) : 134 -143 . DOI: 10.11983/CBB22232

Abstract

The secondary metabolites produced by plants provide human beings with a wealth of pharmaceutical, perfume and industrial raw materials. With the rapid development of molecular biology and genomics research, the biosynthetic gene clusters (BGCs) of secondary metabolites of various plants have been analyzed, which opens a new path for us to quickly obtain the biosynthetic pathways of target products and discover novel natural products. This paper focuses on the definition and characteristics of plant secondary metabolite biosynthesis gene clusters, and its basic structural models, evolution and regulatory mechanisms, in order to provide theoretical basis and reference for related research.

参考文献

[1] 方荣俊, 赵华, 廖永辉, 汤程贻, 吴凤瑶, 朱煜, 庞延军, 陆桂华, 王小明, 杨荣武, 戚金亮, 杨永华 (2014). 乙烯对植物次生代谢产物合成的双重调控效应. 植物学报 49, 626-639.
[2] 吕海舟, 刘琬菁, 何柳, 徐志超, 罗红梅 (2017). 植物次生代谢基因簇研究进展. 植物科学学报 35, 609-621.
[3] 杨谦, 程伯涛, 汤志军, 刘文 (2021). 基因组挖掘在天然产物发现中的应用和前景. 合成生物学 2, 697-715.
[4] Bharadwaj R, Kumar SR, Sharma A, Sathishkumar R (2021). Plant metabolic gene clusters: evolution, organization, and their applications in synthetic biology. Front Plant Sci 12, 697318.
[5] Biere A, Marak HB, van Damme JMM (2004). Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140, 430-441.
[6] Blin K, Shaw S, Steinke K, Villebro R, Ziemert N, Lee SY, Medema MH, Weber T (2019). antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47, W81-W87.
[7] Boutanaev AM, Moses T, Zi JC, Nelson DR, Mugford ST, Peters RJ, Osbourn A (2015). Investigation of terpene diversification across multiple sequenced plant genomes. Proc Natl Acad Sci USA 112, E81-E88.
[8] Chomicki G, Schaefer H, Renner SS (2020). Origin and domestication of Cucurbitaceae crops: insights from phylogenies, genomics and archaeology. New Phytol 226, 1240-1255.
[9] Darbani B, Motawia MS, Olsen CE, Nour-Eldin HH, M?ller BL, Rook F (2016). The biosynthetic gene cluster for the cyanogenic glucoside dhurrin in Sorghum bicolor contains its co-expressed vacuolar MATE transporter. Sci Rep 6, 37079.
[10] Field B, Fiston-Lavier AS, Kemen A, Geisler K, Quesne-ville H, Osbourn AE (2011). Formation of plant metabolic gene clusters within dynamic chromosomal regions. Proc Natl Acad Sci USA 108, 16116-16121.
[11] Field B, Osbourn AE (2008). Metabolic diversification-independent assembly of operon-like gene clusters in different plants. Science 320, 543-547.
[12] Frey M, Chomet P, Glawischnig E, Stettner C, Grun S, Winklmair A, Eisenreich W, Bacher A, Meeley RB, Briggs SP, Simcox K, Gierl A (1997). Analysis of a chemical plant defense mechanism in grasses. Science 277, 696-699.
[13] Gaquerel E, Gulati J, Baldwin IT (2014). Revealing insect herbivory-induced phenolamide metabolism: from single genes to metabolic network plasticity analysis. Plant J 79, 679-692.
[14] Ghanbarian AT, Hurst LD (2015). Neighboring genes show correlated evolution in gene expression. Mol Biol Evol 32, 1748-1766.
[15] Guo L, Winzer T, Yang XF, Li Y, Ning ZM, He ZS, Teodor R, Lu Y, Bowser TA, Graham IA, Ye K (2018). The opium poppy genome and morphinan production. Science 362, 343-347.
[16] Guo LB, Qiu J, Ye CY, Jin GL, Mao LF, Zhang HQ, Yang XF, Peng Q, Wang YY, Jia L, Lin ZX, Li GM, Fu F, Liu C, Chen L, Shen EH, Wang WD, Chu QJ, Wu DY, Wu SL, Xia CY, Zhang YF, Zhou XM, Wang LF, Wu LM, Song WJ, Wang YF, Shu QY, Aoki D, Yumoto E, Yokota T, Miyamoto K, Okada K, Kim DS, Cai DG, Zhang CL, Lou YG, Qian Q, Yamaguchi H, Yamane H, Kong CH, Timko MP, Bai LY, Fan LJ (2017). Echinochloa crusgalli genome analysis provides insight into its adaptation and invasiveness as a weed. Nat Commun 8, 1031.
[17] Haralampidis K, Bryan G, Qi X, Papadopoulou K, Bakht S, Melton R, Osbourn A (2001). A new class of oxidosqualene cyclases directs synthesis of antimicrobial phytoprotectants in monocots. Proc Natl Acad Sci USA 98, 13431-13436.
[18] Hen-Avivi S, Savin O, Racovita RC, Lee WS, Adamski NM, Malitsky S, Almekias-Siegl E, Levy M, Vautrin S, Bergès H, Friedlander G, Kartvelishvily E, Ben-Zvi G, Alkan N, Uauy C, Kanyuka K, Jetter R, Distelfeld A, Aharoni A (2016). A metabolic gene cluster in the wheat W1 and the barley Cer-cqu loci determines β-diketone biosynthesis and glaucousness. Plant Cell 28, 1440-1460.
[19] Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R, Tikunov Y, Bovy A, Chikate Y, Singh P, Rogachev I, Beekwilder J, Giri AP, Aharoni A (2013). Biosynthesis of antinutritional alkaloids in solanaceous crops is mediated by clustered genes. Science 341, 175-179.
[20] Jeon JE, Kim JG, Fischer CR, Mehta N, Dufour-Schroif C, Wemmer K, Mudgett MB, Sattely E (2020). A pathogen-responsive gene cluster for highly modified fatty acids in tomato. Cell 180, 176-187.
[21] Jonczyk R, Schmidt H, Osterrieder A, Fiesselmann A, Schullehner K, Haslbeck M, Sicker D, Hofmann D, Yalpani N, Simmons C, Frey M, Gierl A (2008). Elucidation of the final reactions of DIMBOA-glucoside biosynthesis in maize: characterization of Bx6 and Bx7. Plant Physiol 146, 1053-1063.
[22] Jones DA (1998). Why are so many food plants cyanogenic? Phytochemistry 47, 155-162.
[23] Kakes P (1989). An analysis of the costs and benefits of the cyanogenic system in Trifolium repens L. Theor Appl Genet 77, 111-118.
[24] Kariya K, Ube N, Ueno M, Teraishi M, Okumoto Y, Mori N, Ueno K, Ishihara A (2020). Natural variation of diterpenoid phytoalexins in cultivated and wild rice species. Phytochemistry 180, 112518.
[25] Komaki H, Sakurai K, Hosoyama A, Kimura A, Igarashi Y, Tamura T (2018). Diversity of nonribosomal peptide synthetase and polyketide synthase gene clusters among taxonomically close Streptomyces strains. Sci Rep 8, 6888.
[26] Li DD, Bi XY, Ma JJ, Zhang XH, Jiang KN, Zhu XZ, Huang JG, Zhou LJ (2022). Natural herbicidal alkaloid berberine regulates the expression of thalianol and marneral gene clusters in Arabidopsis thaliana. Pest Manag Sci 78, 2896-2908.
[27] Li DP, Gaquerel E (2021). Next-generation mass spectrometry metabolomics revives the functional analysis of plant metabolic diversity. Annu Rev Plant Biol 72, 867-891.
[28] Liu ZH, Suarez Duran HG, Harnvanichvech Y, Stephenson MJ, Schranz ME, Nelson D, Medema MH, Osbourn A (2020). Drivers of metabolic diversification: how dynamic genomic neighbourhoods generate new biosynthetic pathways in the Brassicaceae. New Phytol 227, 1109-1123.
[29] Luo C, Fernie AR, Yan JB (2020). Single-cell genomics and epigenomics: technologies and applications in plants. Trends Plant Sci 25, 1030-1040.
[30] Matsuba Y, Nguyen TTH, Wiegert K, Falara V, Gonzales-Vigil E, Leong B, Sch?fer P, Kudrna D, Wing RA, Bolger AM, Usadel B, Tissier A, Fernie AR, Barry CS, Pichersky E (2013). Evolution of a complex locus for terpene biosynthesis in Solanum. Plant Cell 25, 2022-2036.
[31] Nelson D, Werck-Reichhart D (2011). A P450-centric view of plant evolution. Plant J 66, 194-211.
[32] Netzker T, Fischer J, Weber J, Mattern DJ, K?nig CC, Valiante V, Schroeckh V, Brakhage AA (2015). Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol 6, 299.
[33] Nützmann HW, Doerr D, Ramírez-Colmenero A, Sotelo- Fonseca JE, Wegel E, Di Stefano M, Wingett SW, Fraser P, Hurst L, Fernandez-Valverde SL, Osbourn A (2020). Active and repressed biosynthetic gene clusters have spatially distinct chromosome states. Proc Natl Acad Sci USA 117, 13800-13809.
[34] Nützmann HW, Huang AC, Osbourn A (2016). Plant metabolic clusters—from genetics to genomics. New Phytol 211, 771-789.
[35] Nützmann HW, Osbourn A (2014). Gene clustering in plant specialized metabolism. Curr Opin Biotechnol 26, 91-99.
[36] Nützmann HW, Scazzocchio C, Osbourn A (2018). Metabolic gene clusters in eukaryotes. Annu Rev Genet 52, 159-183.
[37] Okada BK, Wu YH, Mao DN, Bushin LB, Seyedsayam-dost MR (2016). Mapping the trimethoprim-induced secondary metabolome of Burkholderia thailandensis. ACS Chem Biol 11, 2124-2130.
[38] Osbourn A (2010). Secondary metabolic gene clusters: evolutionary toolkits for chemical innovation. Trends Genet 26, 449-457.
[39] Park HL, Kim TL, Bhoo SH, Lee TH, Lee SW, Cho MH (2018). Biochemical characterization of the rice cinnamyl alcohol dehydrogenase gene family. Molecules 23, 2659.
[40] Qi X, Bakht S, Qin B, Leggett M, Hemmings A, Mellon F, Eagles J, Werck-Reichhart D, Schaller H, Lesot A, Melton R, Osbourn A (2006). A different function for a member of an ancient and highly conserved cytochrome P450 family: from essential sterols to plant defense. Proc Natl Acad Sci USA 103, 18848-18853.
[41] Qi XQ, Bakht S, Leggett M, Maxwell C, Melton R, Osbourn A (2004). A gene cluster for secondary metabolism in oat: implications for the evolution of metabolic diversity in plants. Proc Natl Acad Sci USA 101, 8233-8238.
[42] Roddick JG, Weissenberg M, Leonard AL (2001). Membrane disruption and enzyme inhibition by naturally-occurring and modified chacotriose-containing Solanum steroidal glycoalkaloids. Phytochemistry 56, 603-610.
[43] Rokas A, Mead ME, Steenwyk JL, Raja HA, Oberlies NH (2020). Biosynthetic gene clusters and the evolution of fungal chemodiversity. Nat Prod Rep 37, 868-878.
[44] Rokas A, Wisecaver JH, Lind AL (2018). The birth, evolution and death of metabolic gene clusters in fungi. Nat Rev Microbiol 16, 731-744.
[45] Schneider LM, Adamski NM, Christensen CE, Stuart DB, Vautrin S, Hansson M, Uauy C, von Wettstein-Knowles P (2016). The Cer-cqu gene cluster determines three key players in a β-diketone synthase polyketide pathway synthesizing aliphatics in epicuticular waxes. J Exp Bot 67, 2715-2730.
[46] Shang Y, Ma YS, Zhou Y, Zhang HM, Duan LX, Chen HM, Zeng JG, Zhou Q, Wang SH, Gu WJ, Liu M, Ren JW, Gu XF, Zhang SP, Wang Y, Yasukawa K, Bouwmeester HJ, Qi XQ, Zhang ZH, Lucas WJ, Huang SW (2014). Biosynthesis, regulation, and domestication of bitterness in cucumber. Science 346, 1084-1088.
[47] Shen SQ, Peng M, Fang H, Wang ZX, Zhou S, Jing XY, Zhang M, Yang CK, Guo H, Li YF, Lei L, Shi YH, Sun YY, Liu XQ, Xu CP, Tohge T, Yuan M, Fernie AR, Ning YS, Wang GL, Luo J (2021). An Oryza-specific hydroxycinnamoyl tyramine gene cluster contributes to enhanced disease resistance. Sci Bull 66, 2369-2380.
[48] Smith DJ, Burnham MKR, Edwards J, Earl AJ, Turner G (1990). Cloning and heterologous expression of the penicillin biosynthetic gene cluster from Penicillium chrysogenum. Biotechnology 8, 39-41.
[49] Takos AM, Knudsen C, Lai D, Kannangara R, Mikkelsen L, Motawia MS, Olsen CE, Sato S, Tabata S, J?rgensen K, M?ller BL, Rook F (2011). Genomic clustering of cyanogenic glucoside biosynthetic genes aids their identification in Lotus japonicus and suggests the repeated evolution of this chemical defence pathway. Plant J 68, 273-286.
[50] Tao HY, Zuo L, Xu HL, Li C, Qiao G, Guo MY, Lin XK (2020). Alkaloids as anticancer agents: a review of Chinese patents in recent 5 years. Recent Pat Anticancer Drug Discov 15, 2-13.
[51] Tattersall DB, Bak S, Jones PR, Olsen CE, Nielsen JK, Hansen ML, H?j PB, M?ller BL (2001). Resistance to an herbivore through engineered cyanogenic glucoside synthesis. Science 293, 1826-1828.
[52] Tunyasuvunakool K, Adler J, Wu Z, Green T, Zielinski M, ?ídek A, Bridgland A, Cowie A, Meyer C, Laydon A, Velankar S, Kleywegt GJ, Bateman A, Evans R, Pritzel A, Figurnov M, Ronneberger O, Bates R, Kohl SAA, Potapenko A, Ballard AJ, Romera-Paredes B, Nikolov S, Jain R, Clancy E, Reiman D, Petersen S, Senior AW, Kavukcuoglu K, Birney E, Kohli P, Jumper J, Hassabis D (2021). Highly accurate protein structure prediction for the human proteome. Nature 596, 590-596.
[53] Varshney RK, Bohra A, Yu JM, Graner A, Zhang QF, Sorrells ME (2021). Designing future crops: genomics- assisted breeding comes of age. Trends Plant Sci 26, 631-649.
[54] Verpoorte R, Memelink J (2002). Engineering secondary metabolite production in plants. Curr Opin Biotechnol 13, 181-187.
[55] von Rad U, Hüttl R, Lottspeich F, Gierl A, Frey M (2001). Two glucosyltransferases are involved in detoxification of benzoxazinoids in maize. Plant J 28, 633-642.
[56] Vranová E, Coman D, Gruissem W (2013). Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64, 665-700.
[57] Weber T, Kim HU (2016). The secondary metabolite bioinformatics portal: computational tools to facilitate synthetic biology of secondary metabolite production. Synth Syst Biotechnol 1, 69-79.
[58] Winzer T, Gazda V, He ZS, Kaminski F, Kern M, Larson TR, Li Y, Meade F, Teodor R, Vaistij FE, Walker C, Bowser TA, Graham IA (2012). A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336, 1704-1708.
[59] Wu X, Feng H, Wu D, Yan SJ, Zhang P, Wang WB, Zhang J, Ye JL, Dai GX, Fan Y, Li WK, Song BX, Geng ZD, Yang WL, Chen GX, Qin F, Terzaghi W, Stitzer M, Li L, Xiong LZ, Yan JB, Buckler E, Yang WN, Dai MQ (2021). Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance. Genome Biol 22, 185.
[60] Wu S, Morotti AL, Wang SS, Wang Y, Xu XY, Chen JH, Wang GD, Tatsis EC (2022). Convergent gene clusters underpin hyperforin biosynthesis in St John’s wort. New Phytol 235, 646-661.
[61] Xu MM, Galhano R, Wiemann P, Bueno E, Tiernan M, Wu W, Chung IM, Gershenzon J, Tudzynski B, Sesma A, Peters RJ (2012). Genetic evidence for natural product-mediated plant-plant allelopathy in rice (Oryza sativa). New Phytol 193, 570-575.
[62] Yamamuro C, Zhu JK, Yang ZB (2016). Epigenetic modifications and plant hormone action. Mol Plant 9, 57-70.
[63] Yang WN, Feng H, Zhang XH, Zhang J, Doonan JH, Batchelor WD, Xiong LZ, Yan JB (2020). Crop phenomics and high-throughput phenotyping: past decades, current challenges, and future perspectives. Mol Plant 13, 187-214.
[64] Yang XF, Gao SH, Guo L, Wang B, Jia YY, Zhou J, Che YZ, Jia P, Lin JD, Xu T, Sun JY, Ye K (2021). Three chromosome-scale Papaver genomes reveal punctuated patchwork evolution of the morphinan and noscapine biosynthesis pathway. Nat Commun 12, 6030.
[65] Yu N, Nützmann HW, MacDonald JT, Moore B, Field B, Berriri S, Trick M, Rosser SJ, Kumar SV, Freemont PS, Osbourn A (2016). Delineation of metabolic gene clusters in plant genomes by chromatin signatures. Nucleic Acids Res 44, 2255-2265.
[66] Yue JP, Hu XY, Huang JL (2013). Horizontal gene transfer in the innovation and adaptation of land plants. Plant Signal Behav 8, e24130.
[67] Zhan CS, Lei L, Liu ZX, Zhou S, Yang CK, Zhu XT, Guo H, Zhang F, Peng M, Zhang M, Li YF, Yang ZX, Sun YY, Shi YH, Li K, Liu L, Shen SQ, Wang XY, Shao JW, Jing XY, Wang ZX, Li Y, Czechowski T, Hasegawa M, Graham I, Tohge T, Qu LH, Liu XQ, Fernie AR, Chen LL, Yuan M, Luo J (2020). Selection of a subspecies-specific diterpene gene cluster implicated in rice disease resistance. Nat Plants 6, 1447-1454.
[68] Zhan CS, Shen SQ, Yang CK, Liu ZH, Fernie AR, Graham IA, Luo J (2022). Plant metabolic gene clusters in the multiomics era. Trends Plant Sci 27, 981-1001.
[69] Zhu GT, Wang SC, Huang ZJ, Zhang SB, Liao QG, Zhang CZ, Lin T, Qin M, Peng M, Yang CK, Cao X, Han X, Wang XX, van der Knaap E, Zhang ZH, Cui X, Klee H, Fernie AR, Luo J, Huang SW (2018). Rewiring of the fruit metabolome in tomato breeding. Cell 172, 249-261.
文章导航

/