Transcription Factor MYCs Regulating Terpenoids in Tomato Trichomes: Research Progress on Molecular Mechanism

doi:10.11924/j.issn.1000-6850.casb2021-0346

Abstract

Abstract:

Tomato is an important vegetable widely grown worldwide, and it is susceptible to pests and diseases, resulting in the reduction of yield. Trichome is a crucial barrier covering the epidermis of tomato, which can enhance the adaptability of tomato to biotic and abiotic stresses. In order to further study the functional mechanism of trichomes in tomato stress resistance, the types of tomato trichome inclusions and molecular regulation mechanism were summarized in this review, and the molecular mechanism of the terpenoids’ synthesis regulation in tomato trichomes by the core transcription factor MYC1 and MYC2 in JA signaling pathway was concluded. The problems existing in the current trichome research were analyzed, and the future research direction of trichome was discussed.

Key words: JA signaling, regulating mechanism, tomato trichome, terpenoids, SlMYC1/2, transcription factor

CLC Number:

S626.5

YU Lan, WANG Haoran, ZHANG Ying, XING Hongyun, DING Qi, ZHAO Baozhen, CUI Na. Transcription Factor MYCs Regulating Terpenoids in Tomato Trichomes: Research Progress on Molecular Mechanism[J]. Chinese Agricultural Science Bulletin, 2022, 38(6): 87-93.

Figures/Tables 2

References 73

[1]	HUCHELMANN A, BOUTRY M, HACHEZ C. Plant glandular trichomes: natural cell factories of high biotechnological interest[J]. Plant physiology, 2017, 175(1):6-22. doi: 10.1104/pp.17.00727 URL
[2]	LIU X, BARTHOLOMEW E, CAI Y, et al. Trichome-related mutants provide a new perspective on multicellular trichome initiation and development in cucumber (Cucumis sativus L.)[J]. Frontiers in plant science, 2016, 7:1187.
[3]	HAUSER M T. Molecular basis of natural variation and environmental control of trichome patterning[J]. Frontiers in Plant Science, 2014, 5(5):320.
[4]	OCHOA-LÓPEZ S, DAMIÁN X, REBOLLO R, et al. Ontogenetic changes in the targets of natural selection in three plant defenses[J]. New phytologist, 2020, 226(5):1480-1491. doi: 10.1111/nph.v226.5 URL
[5]	KENNEDY G G. Tomato, pests, parasitoids, and predators: tritrophic interactions involving the genus Lycopersicon[J]. Annual review of entomology, 2003, 48(1):51-72. doi: 10.1146/ento.2003.48.issue-1 URL
[6]	KARIYAT R R, SMITH J D, STEPHENSON A G, et al. Non-glandular trichomes of Solanum carolinense deter feeding by Manduca sexta caterpillars and cause damage to the gut peritrophic matrix[J]. Proceedings of the royal society b: biological sciences, 2017, 284(1849):20162323.
[7]	TIAN D, TOOKER J, PEIFFER M, et al. Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum)[J]. Planta, 2012, 236(4):1053-1066. doi: 10.1007/s00425-012-1651-9 URL
[8]	FRIDMAN E, WANG J, IIJIMA Y, et al. Metabolic, genomic, and biochemical analyses of glandular trichomes from the wild tomato species Lycopersicon hirsutum identify a key enzyme in the biosynjournal of methylketones[J]. Plant cell, 2005, 17(4):1252-1267. doi: 10.1105/tpc.104.029736 URL
[9]	LUU V T, WEINHOLD A, ULLAH C, et al. O-acyl sugars protect a wild tobacco from both native pungal pathogens and a specialist herbivore[J]. Plant physiology, 2017:370-386.
[10]	ENYA J, SHINOHARA H, YOSHIDA S, et al. Culturable leaf-associated bacteria on tomato plants and their potential as biological control agents[J]. Microbial ecology, 2007, 53(4):524-536. doi: 10.1007/s00248-006-9085-1 URL
[11]	TANG T, LI C H, LI D S, et al. Peltate glandular trichomes of Colquhounia vestita harbor diterpenoid acids that contribute to plant adaptation to UV radiation and cold stresses[J]. Phytochemistry, 2020, 172:112285. doi: 10.1016/j.phytochem.2020.112285 URL
[12]	ASHFAQ S, AHMAD M, ZAFAR M, et al. Foliar micromorphology of convolvulaceous species with special emphasis on trichome diversity from the arid zone of Pakistan[J]. Flora, 2019, 255:110-124. doi: 10.1016/j.flora.2019.04.007 URL
[13]	GALDON-ARMERO J, FULLANA-PERICAS M, MULET P A, et al. The ratio of trichomes to stomata is associated with water use efficiency in tomato[J]. Plant journal for cell & molecular biology, 2018, 96(3):607-619.
[14]	PROZHERINA N, FREIWALD V, OKSANEN R E. Interactive effect of springtime frost and elevated ozone on early growth, foliar injuries and leaf structure of birch (Betula pendula)[J]. New phytologist, 2003, 159(3):623-636. doi: 10.1046/j.1469-8137.2003.00828.x URL
[15]	SLETVOLD N, HUTTUNEN P, HANDLEY R, et al. Cost of trichome production and resistance to a specialist insect herbivore in Arabidopsis lyrata[J]. Evolutionary ecology, 2010, 24(6):1307-1319. doi: 10.1007/s10682-010-9381-6 URL
[16]	BALCKE G U, BENNEWITZ S, BERGAU N, et al. Multi-omics of tomato glandular trichomes reveals distinct features of central carbon metabolism supporting high productivity of specialized metabolites[J]. Plant cell, 2017, 29(5):960-983. doi: 10.1105/tpc.17.00060 URL
[17]	YANG C X, YE Z B. Trichomes as models for studying plant cell differentiation[J]. Cellular and molecular life sciences, 2013, 70(11):1937-1948. doi: 10.1007/s00018-012-1147-6 URL
[18]	ZHANG B, CHOPRA D, SCHRADER A, et al. Evolutionary comparison of competitive protein-complex formation of MYB, bHLH, and WDR proteins in plants[J]. Journal of experimental botany, 2019, 70(12):3197-3209. doi: 10.1093/jxb/erz155 URL
[19]	HUNG F Y, CHEN J H, FENG Y R, et al. Arabidopsis JMJ29 is involved in trichome development by regulating the core trichome initiation gene GLABRA3[J]. Plant journal, 2020, 103(5):1735-1743. doi: 10.1111/tpj.v103.5 URL
[20]	PERES A, CHURCHMAN M L, HARIHARAN S, et al. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses[J]. Journal of biological chemistry, 2007, 282(35):25588-25596. doi: 10.1074/jbc.M703326200 URL
[21]	MOROHASHI K, GROTEWOLD E. A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors[J]. PLoS genetics, 2009, 5(2):e1000396.
[22]	BRAMSIEPE J, WESTER K, WEINL C, et al. Endoreplication controls cell fate maintenance[J]. PLoS genetics, 2010, 6(6):e1000996.
[23]	SCHELLMANN S, SCHNITTGER A, KIRIK V, et al. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis[J]. The EMBO journal, 2002, 21(19):5036-5046. doi: 10.1093/emboj/cdf524 URL
[24]	PATTANAIK S, PATRA B, SINGH S K, et al. An overview of the gene regulatory network controlling trichome development in the model plant, Arabidopsis[J]. Frontiers in plant science, 2014, 5:259.
[25]	PAYNE T, CLEMENT J, ARNOLD D, et al. Heterologous myb genes distinct from GL1 enhance trichome production when overexpressed in Nicotiana tabacum[J]. Development, 1999, 126(4):671-682. doi: 10.1242/dev.126.4.671 URL
[26]	SERNA L, MARTIN C. Trichomes: different regulatory networks lead to convergent structures[J]. Trends in plant science, 2006, 11(6):274-280. doi: 10.1016/j.tplants.2006.04.008 URL
[27]	GAO Y, LIU J, CHEN Y, et al. Tomato SlAN11 regulates flavonoid biosynjournal and seed dormancy by interaction with bHLH proteins but not with MYB proteins[J]. Horticulture research, 2018, 5(1):27. doi: 10.1038/s41438-018-0032-3 URL
[28]	YING S, SU M, WU Y, et al. Trichome regulator SlMIXTA-like directly manipulates primary metabolism in tomato fruit[J]. Plant biotechnology journal, 2020, 18(2):354-363. doi: 10.1111/pbi.v18.2 URL
[29]	CHANG J, XU Z, LI M, et al. Spatiotemporal cytoskeleton organizations determine morphogenesis of multicellular trichomes in tomato[J]. PLoS genetics, 2019, 15(10):e1008438.
[30]	LIU S, ZHANG Y, FENG Q, et al. Tomato AUXIN RESPONSE FACTOR 5 regulates fruit set and development via the mediation of auxin and gibberellin signaling[J]. Sentific reports, 2018, 8(1):2971.
[31]	CHALVIN C, DREVENSEK S, DRON M, et al. Genetic control of glandular trichome development[J]. Trends in plant science, 2020, 25(5):477-487. doi: 10.1016/j.tplants.2019.12.025 URL
[32]	EWAS M, GAO Y, ALI F, et al. RNA-seq reveals mechanisms of SlMX1 for enhanced carotenoids and terpenoids accumulation along with stress resistance in tomato[J]. Science bulletin, 2017(7):476-485.
[33]	CHANG J, YU T, YANG Q, et al. Hair, encoding a single C₂H₂ zinc-finger protein, regulates multicellular trichome formation in tomato[J]. The plant journal, 2018, 96(1):90-102. doi: 10.1111/tpj.14018 URL
[34]	YU X, CHEN G, TANG B, et al. The Jasmonate ZIM-domain protein gene SlJAZ2 regulates plant morphology and accelerates flower initiation in Solanum lycopersicum plants[J]. Plant science an international journal of experimental plant biology, 2018, 267:65.
[35]	CHEN Y, SU D, LI J, et al. Overexpression of SlbHLH95, a basic helix-loop-helix transcription factor family member, impacts trichome formation via regulating gibberellin biosynjournal in tomato[J]. Journal of experimental botany, 2020, 71(12):3450-3462. doi: 10.1093/jxb/eraa114 URL
[36]	WEI D, YANG Y, REN Z, et al. The tomato SlIAA15 is involved in trichome formation and axillary shoot development[J]. New phytologist, 2012, 194(2):379-390. doi: 10.1111/nph.2012.194.issue-2 URL
[37]	KAWAGUCHI S, MIMURA M, OHYA T, et al. Hormone-mediated pattern formation in seedling of plants: a competitive growth dynamics model[J]. Journal of the physical society of Japan, 2003, 70(10):3155-3160. doi: 10.1143/JPSJ.70.3155 URL
[38]	GLAS J J, SCHIMMEL B C, ALBA J M, et al. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores[J]. International journal of molecular sciences, 2012, 13(12):17077-17103. doi: 10.3390/ijms131217077 URL
[39]	SIMMONS A T, GURR G M, MCGRATH D, et al. Entrapment of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) on glandular trichomes of Lycopersicon species[J]. Australian journal of entomology, 2004, 43(2):196-200. doi: 10.1111/aen.2004.43.issue-2 URL
[40]	VENDEMIATTI E, ZSÖGÖN A, SILVA G F F E, et al. Loss of type-IV glandular trichomes is a heterochronic trait in tomato and can be reverted by promoting juvenility[J]. Plant science, 2017, 259:35-47. doi: 10.1016/j.plantsci.2017.03.006 URL
[41]	SIMMONS A T, GURR G M. Trichomes of Lycopersicon species and their hybrids: effects on pests and natural enemies[J]. Agricultural & forest entomology, 2010, 7(4):265-276.
[42]	CHANG J, XU Z, LI M, et al. Spatiotemporal cytoskeleton organizations determine morphogenesis of multicellular trichomes in tomato[J]. PLoS genetics, 2019, 15(10):e1008438. doi: 10.1371/journal.pgen.1008438 URL
[43]	YANAGISAWA M, DESYATOVA A S, BELTETON S A, et al. Patterning mechanisms of cytoskeletal and cell wall systems during leaf trichome morphogenesis[J]. Nature plants, 2015, 1(3):15014. doi: 10.1038/nplants.2015.14 URL
[44]	ZHANG Y, SONG H, WANG X, et al. The roles of different types of trichomes in tomato resistance to cold, drought, whiteflies, and botrytis[J]. Agronomy, 2020, 10(3):411. doi: 10.3390/agronomy10030411 URL
[45]	MCDOWELL E T, KAPTEYN J, SCHMIDT A, et al. Comparative functional genomic analysis of Solanum glandular trichome types[J]. Plant physiology, 2011, 155(1):524-539. doi: 10.1104/pp.110.167114 URL
[46]	WILLIAMS W G, KENNEDY G G, YAMAMOTO R T, et al. 2-tridecanone: a naturally occurring insecticide from the wild tomato Lycopersicon hirsutum f. glabratum[J]. Science, 1999, 207:888-889. doi: 10.1126/science.207.4433.888 URL
[47]	SCHMIDT A, LI C, SHI F, et al. Polymethylated myricetin in trichomes of the wild tomato species Solanum habrochaites and characterization of trichome-specific 3’/5’-and 7/4’-myricetin O-methyltransferases[J]. Plant physiology, 2011, 155(4):1999-2009. doi: 10.1104/pp.110.169961 URL
[48]	ZHOU F, PICHERSKY E. The complete functional characterisation of the terpene synthase family in tomato[J]. New phytologist, 2020, 226(5):1341-1360. doi: 10.1111/nph.v226.5 URL
[49]	ABBAS F, KE Y, YU R, et al. Volatile terpenoids: multiple functions, biosynjournal, modulation and manipulation by genetic engineering[J]. Planta, 2017, 246(5):803-816. doi: 10.1007/s00425-017-2749-x URL
[50]	CHEN G, KLINKHAMER P G L, ESCOBAR-BRAVO R, et al. Type VI glandular trichome density and their derived volatiles are differently induced by jasmonic acid in developing and fully developed tomato leaves: implications for thrips resistance[J]. Plant sicence, 2018, 276:87-98.
[51]	CHEN M, GUO H, CHEN S, et al. Methyl jasmonate promotes phospholipid remodeling and jasmonic acid signaling to alleviate chilling injury in peach fruit[J]. Journal of agricultural and food chemistry, 2019, 67(35):1-39. doi: 10.1021/acs.jafc.8b06672 URL
[52]	ALI A Y A, IBRAHIM M E H, ZHOU G, et al. Exogenous jasmonic acid and humic acid increased salinity tolerance of sorghum[J]. Agronomy journal, 2020, 112(2):871-884. doi: 10.1002/agj2.v112.2 URL
[53]	COELHO D G, DE ANDRADE H M, MARINATO C S, et al. Exogenous jasmonic acid enhances oxidative protection of Lemna valdiviana subjected to arsenic[J]. Acta physiologiae plantarum, 2020, 42(97):97. doi: 10.1007/s11738-020-03086-0 URL
[54]	CHINI A, GIMENEZ I S, GOOSSENS A, et al. Redundancy and specificity in jasmonate signalling[J]. Current Opinion in Plant Biology, 2016, 33:147-156. doi: 10.1016/j.pbi.2016.07.005 URL
[55]	GOOSSENS J, FERNÁNDEZ-CALVO P, SCHWEIZER F, et al. Jasmonates: signal transduction components and their roles in environmental stress responses[J]. Plant molecular biology, 2016, 91:673-689. doi: 10.1007/s11103-016-0480-9 URL
[56]	XU J, VAN HERWIJNEN Z O, DRÄGER D B, et al. SlMYC1 regulates type VI glandular trichome formation and terpene biosynjournal in tomato glandular cells[J]. Plant cell, 2018, 30(12):2988-3005. doi: 10.1105/tpc.18.00571 URL
[57]	LIU Y, DU M, DENG L, et al. MYC2 regulates the termination of jasmonate signaling via an autoregulatory negative feedback loop[J]. Plant cell, 2019, 31(1):106-127. doi: 10.1105/tpc.18.00405 URL
[58]	MIN D, LI F, CUI X, et al. SlMYC2 are required for methyl jasmonate-induced tomato fruit resistance to Botrytis cinerea[J]. Food chemistry, 2019, 310:125901. doi: 10.1016/j.foodchem.2019.125901 URL
[59]	ZHANG F, YAO J, KE J, et al. Structural basis of JAZ repression of MYC transcription factors in jasmonate signalling[J]. Nature, 2015, 525:269-273. doi: 10.1038/nature14661 URL
[60]	MAJOR I T, YOSHIDA Y, CAMPOS M L, et al. Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module[J]. New phytologist, 2017, 215(4):1533-1547. doi: 10.1111/nph.2017.215.issue-4 URL
[61]	DU M, ZHAO J, TZENG D T W, et al. MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato[J]. Plant cell, 2017, 29(8):1883-1906. doi: 10.1105/tpc.16.00953 URL
[62]	PAUWELS L, BARBERO G F, GEERINCK J, et al. NINJA connects the co-repressor TOPLESS to jasmonate signalling[J]. Nature, 2010, 464:788-791. doi: 10.1038/nature08854 URL
[63]	GARRIDO-BIGOTES A, VALENZUELA-RIFFO F, TORREJÓN M, et al. A new functional JAZ degron sequence in strawberry JAZ1 revealed by structural and interaction studies on the COI1-JA-Ile/COR-JAZs complexes[J]. Scientific reports, 2020, 10(1):1-17. doi: 10.1038/s41598-019-56847-4 URL
[64]	MAJOR I T, YOSHIDA Y, CAMPOS M L, et al. Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module[J]. New phytologist, 2017, 215(4):1533-1547. doi: 10.1111/nph.2017.215.issue-4 URL
[65]	THUROW C, KRISCHKE M, MUELLER M J. Induction of Jasmonoyl-Isoleucine (JA-Ile)-dependent JASMONATE ZIM-DOMAIN (JAZ) genes in NaCl-treated Arabidopsis thaliana roots can occur at very low JA-Ile levels and in the absence of the JA/JA-Ile transporter JAT1/AtABCG16[J]. Plants, 2020, 9(12):1635. doi: 10.3390/plants9121635 URL
[66]	ORTIGOSA A, FONSECA S, FRANCO-ZORRILLA J M, et al. The JA-pathway MYC transcription factors regulate photomorphogenic responses by targeting HY5 gene expression[J]. Plant journal, 2019, 102(1):138-152. doi: 10.1111/tpj.v102.1 URL
[67]	WANG H, LI S, LI Y, et al. MED25 connects enhancer-promoter looping and MYC2-dependent activation of jasmonate signalling[J]. Nature plants, 2019, 5(6):616-625. doi: 10.1038/s41477-019-0441-9 URL
[68]	AN C, LI L, ZHAI Q, et al. Mediator subunit MED25 links the jasmonate receptor to transcriptionally active chromatin[J]. Proceedings of the national academy of sciences of the United of America, 2017, 114(42):8930-8939.
[69]	CHEN Q, SUN J, ZHAI Q, et al. The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis[J]. Plant cell, 2011, 23(9):3335-3352. doi: 10.1105/tpc.111.089870 URL
[70]	QI T, WANG J, HUANG H, et al. Regulation of jasmonate-induced leaf senescence by antagonism between bHLH subgroup IIIe and IIId factors in Arabidopsis[J]. Plant cell, 2015, 27(6):1634-1649. doi: 10.1105/tpc.15.00110 URL
[71]	LI L, ZHAO Y, MCCAIG B C, et al. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development[J]. Plant Cell, 2004, 16(1):126-143. doi: 10.1105/tpc.017954 URL
[72]	YAN T, LI L, XIE L, et al. A novel HD-ZIP IV/MIXTA complex promotes glandular trichome initiation and cuticle development in Artemisia annua[J]. New phytologist, 2018, 218(2):567-578. doi: 10.1111/nph.15005 URL
[73]	SWINNEN G, DE MEYER M, POLLIER J, et al. Constitutive steroidal glycoalkaloid biosynjournal in tomato is regulated by the clade IIIe basic helix-loop-helix transcription factors MYC1 and MYC2[J]. bioRxiv, 2020. DOI: 10.1101/2020.01.27.921833.

器官	化合物
器官	单萜	倍半萜
叶片	α-蒎烯(α-pinene) 伞花烃(p-cymene) α-水芹烯(α-phellandrene) α-松油烯(α-terpinene) β-水芹烯(β-phellandrene) γ-松油烯(γ-terpinene) 月桂烯(myrcene) δ-蒈烯(δ-carene) 柠檬烯(limonene) 反式罗勒烯(trans-ocimene) 异松油烯(terpinolene)	β-石竹烯(β-caryophyllene) α-石竹烯(α-caryophyllene)
茎	α-蒎烯(α-pinene) 伞花烃(ρ-cymene) α-水芹烯(α-phellandrene) α-松油烯(α-terpinene) β-水芹烯 (β-phellandrene) γ-松油烯(γ-terpinene) 2-蒈烯(2-carene) β-罗勒烯(β-ocimene) 松油烯(terpinolene) D-柠檬烯(D-limonene)	β-石竹烯(β-caryophyllene) α-葎草烯(α-humulene)

器官	化合物
器官	单萜	倍半萜
叶片	α-蒎烯(α-pinene) 伞花烃(p-cymene) α-水芹烯(α-phellandrene) α-松油烯(α-terpinene) β-水芹烯(β-phellandrene) γ-松油烯(γ-terpinene) 月桂烯(myrcene) δ-蒈烯(δ-carene) 柠檬烯(limonene) 反式罗勒烯(trans-ocimene) 异松油烯(terpinolene)	β-石竹烯(β-caryophyllene) α-石竹烯(α-caryophyllene)
茎	α-蒎烯(α-pinene) 伞花烃(ρ-cymene) α-水芹烯(α-phellandrene) α-松油烯(α-terpinene) β-水芹烯 (β-phellandrene) γ-松油烯(γ-terpinene) 2-蒈烯(2-carene) β-罗勒烯(β-ocimene) 松油烯(terpinolene) D-柠檬烯(D-limonene)	β-石竹烯(β-caryophyllene) α-葎草烯(α-humulene)