A comprehensive review on glandular trichomes, gene regulating trichome development and how can we apply gene editing technologies to develop a specific type of trichome type

Introduction

Tomatoes (Solanum lycopersicum L.) are among the most essential vegetable crops globally. They rank as the second most cultivated vegetable in terms of both production and consumption. In recent years, demand for tomatoes has surged due to their rich content of nutritionally valuable carotenoids, fibres, vitamins, and minerals (Amr & Raie, 2022) [2] . Tomatoes are also rich in antioxidants, including beta-carotene, as well as various phenolic compounds such as flavonoids, hydroxycinnamic acid, chlorogenic acid, homovanillic acid, and ferulic acid (Collins et al., 2022) [9] . Terrestrial plants, being anchored in the soil, must continuously adapt to their dynamic and complex environments as they grow and develop (Dahl & Arens, 2020) [10] . One significant adaptation that emerged when plants transitioned from aquatic to terrestrial habitats was the development of epidermal hair-like structures. These specialized structures played a crucial role in helping plants cope with the challenges of land environments, such as water retention, protection from herbivores, and resistance to environmental stressors (Huegel, 2019) [28] . When these structures are present on a plant's aerial organs, they are referred to as trichomes, whereas those found on underground parts are known as root hairs (Doroshkov et al., 2019) [15] . In plants, trichomes are hair-like appendages that emerge from the above-ground epidermal cells and can be either unicellular or multicellular (X. Wang et al., 2021) [67] . Trichomes serve as a protective barrier, defending plants against diseases, herbivores, UV radiation, excessive water loss, and also aiding in seed protection and dispersal (Dhankhar et al., 2023) [14] . Although trichomes are small, they play a crucial role in both plant health by producing terpenoids (Glas et al., 2012) [23] . Tomato plants have seven distinct types of trichomes, which are classified as either glandular or nonglandular (Kaur et al., 2023) [33] . Trichomes are generally categorized based on their structure and function, classifying them as unicellular or multicellular, branched or unbranched, and glandular or non-glandular (Deepa, 2024) [12] . Trichomes also divided into various parts, such as head, star, hook, and scale. Glandular trichomes are usually present in all or part of the subepidermal tissue on the leaf surface (Muravnik, 2020) [45] . The growth of plant trichomes is regulated and coordinated by multiple factors, including environmental conditions, hormonal signals, regulatory genes, and non-coding RNA. These elements work together to influence trichome development, ensuring that plants can adapt to their surroundings and effectively perform their protective and physiological functions (Fambrini & Pugliesi, 2019) [18] . Among these factors, regulatory genes, which include transcription factors and functional genes, play a crucial role in controlling the initiation, growth, and development of trichomes (Wang et al, 2021) [67] .

Glandular trichomes

Glandular trichomes, specialized structures formed from plant epidermal cells, serve a variety of biological functions depending on the plant species (Schuurink & Tissier, 2020) [54] . The glandular trichomes are of 4 types based on shape and function (Bergau et al., 2015) [3] . Type 1 trichome capitate is large and has multicellular stalk and a glandular head (Uzelac et al., 2019) [61] . Type IV trichome (Peltate) is short stalked with a broad, and has multicellular glandular head (Deepa, 2024) [12] . Type VI trichome is capitate is the most abundant glandular type in most of the cultivated tomato variety. Type VII trichome is small capitate trichome is similar to type VI but with a smaller glandular head (Bergau et al., 2015; Guo et al., 2013) [3,24] . These functions include providing biochemical protection through the secretion of secondary metabolites and offering mechanical defence due to their physical characteristics (Tian et al., 2017) [58] . Glandular trichomes (GT) have attracted significant attention due to their potential to produce a wide variety of specialized plant metabolites (Tsugawa et al., 2021) [60] . Trichomes, present in many angiosperms as well as in numerous gymnosperms and bryophytes, are classified into two types: secretory glandular trichomes (glandular trichomes) and non-secretory glandular trichomes (non-glandular trichomes) (Han et al., 2022) [25] . Secretory or glandular trichomes produce and secrete secondary metabolites, including terpenes, acyl sugars, and phenolic compounds, which provide chemical defence against herbivores and pathogens (Al-Khayri et al., 2023) [1] . Glandular trichomes also provides defence against biotic and abiotic stresses (Kundan et al., 2019) [40] . Nonglandular or non-secretory trichomes do not secrete substances but serve as physical barriers against biotic and abiotic stress factors (Zhang et al, 2021) [76] .

Role of glandular trichomes in abiotic stress tolerance in tomato

Unfavourable environmental conditions, including biotic and abiotic stress, can inhibit plant growth, development, and reproduction (Chaudhry & Sidhu, 2022) [7] . Biotic stress responses in plants can be triggered by various factors, including insects, other herbivores, viruses, and microbes. In contrast, abiotic stressors encompass environmental conditions such as UV radiation, heavy metals, extreme temperatures (cold and heat), salinity, and drought (Jan et al., 2021) [29] . The glandular trichomes secrete substances like polyphenols or acyl sugars, which can trap insects and lead to their ingestion of toxins or cause them to choke to death (F. Wang et al., 2022) [65] . UV-B radiation stimulates the expression of the trichome-initiation gene GL3, leading to an increased density of leaf trichomes, which helps reflect more light and reduce transpiration (Rai & Agrawal, 2023) [50] . Trichomes play a crucial role in protecting plants from UV-B radiation. Mutants with a higher number of trichomes than the wild type show increased resistance to UV-B, while mutants with fewer trichomes are more susceptible to UV-B damage (Karabourniotis et al., 2020) [31] . Additionally, plants with lower densities of glandular trichomes are more susceptible to ozone stress and the damaging effects of ozone compared to the wild type (Nowroz et al., 2023) [47] . Glandular trichomes on the leaf surface act as chemical barriers, neutralizing ozone before it can reach the leaf. This function plays a vital role in reducing ozone toxicity. Therefore, in polluted environments, the presence of leaf trichomes may be a critical factor influencing the distribution of species (Lihavainen et al., 2017; Nowroz et al., 2023) [43,47] . In addition, glandular trichomes help protect plants from the damaging effects of drought and high temperatures (Zhang et al., 2021) [76] . The ability of tomatoes to endure stress is closely linked to the density and types of trichomes present on the plant (Kariyat, 2020) [32] . In tomato plants, glandular trichomes are associated with the production of both volatile and non-volatile secondary metabolites, such as flavonoids, acyl sugars, terpenoids, and phenylpropanoids (Liu et al., 2019) [44] . Allelochemicals present in the glandular trichomes of wild tomato species are diverse and believed to contribute to pest resistance. The three most recognized and likely the most studied groups of these compounds are methyl ketones, sesquiterpenes, and acyl sugars (Labate et al., 2007) [41] . Although research on tomatoes has primarily focused on Hemiptera and Lepidoptera as the main pests, it has been shown that glandular trichomes in wild tomato varieties also provide resistance to other pest taxa (Rakha et al., 2017) [52] . Tomato plants with high densities of glandular trichomes, specifically types IV and VI, exhibit strong resistance to arthropods. This resistance is largely attributed to the presence of allelochemicals, which primarily include tridecanones (methylketones), sesquiterpenes (terpenoids), and acyl sugars. These chemical compounds play a crucial role in deterring herbivorous insects and enhancing the plant's natural defense mechanisms (Escobar-Bravo et al., 2018; Rakha et al., 2017) [16,52] . Trichomes serve as a natural defense mechanism by hindering insect movement and preventing them from biting the plant (Despland, 2019; Watts & Kariyat, 2022) [13,68] . Additionally, tomato glandular trichomes detect insect movement and act as mechanoreceptors, initiating internal responses such as the production of jasmonic acid (JA) and salicylic acid (SA) (Zhang et al., 2021) [76] . The insect becomes trapped in the secretions of glandular trichomes, which produce acyl sugars or polyphenols, forcing it to ingest toxins or suffocate, ultimately leading to its death (NANDI et al., 2022) [46] . However, glandular trichomes can also detect the physical movements of insects and act as mechanoreceptors, triggering internal processes such as the production of jasmonic acid (JA) and salicylic acid (SA) (Zhang et al., 2021) [76] . Solanum habrochaites is one of the most extensively studied wild tomato species for its resistance to arthropods (de Oliveira et al., 2020) [11] . Type IV and VI trichomes in this widely distributed species have demonstrated resistance to more thrips species and aphid species (Blanco-sanchez et al, 2021). Among these, only one entry, PI 134417, has been identified Solanum habrochaites var. Glabratum exhibits resistance to several pests (Savi, 2022) [53] .

Gene regulating trichome development in tomato plant

Glandular trichomes are essential for tomatoes to defend against herbivores (Tabary et al., 2024) [57] . Artemisia annua and tomatoes have both been previously proposed as suitable models for studying the formation of glandular trichomes (Qin et al., 2021) [49] . In Artemisia annua and tomatoes, several transcription factors involved in glandular trichome initiation have been identified, with most belonging to the R2R3-MYB and HD-ZIP IV transcription factor subfamilies. Additionally, certain members of the R2R3-MYB subfamily have been shown to regulate specialized metabolism (R. A. Khan et al., 2021) [36] . R2R3-MYB, along with MIXTA and MIXTA-like genes, play a crucial role in determining the fate of epidermal cells (B. Xu et al., 2021) [71] . The first MIXTA gene was identified in Snapdragon (Antirrhinum majus), where it regulates the differentiation of conical epidermal cells from flat epidermal cells (Qiao et al., 2023) [48] . In tomatoes and Artemisia annua, three members of the R2R3-MYB subfamily have been identified as positive regulators of glandular trichome initiation, including SlMX1 in tomatoes (Ewas et al., 2022) [17] , and AaMYB1 and AaMIXTA1 in Artemisia annua (Chalvin et al., 2019) [6] . Plants of Artemisia annua that overexpress AaMYB1 have been shown to develop a higher density of glandular trichomes (Li et al., 2024) [42] . Additionally, SlMX1 in tomatoes and AaMIXTA1 in Artemisia annua are downregulated (Han et al., 2022). A decrease in the expression of these genes reduces the density of glandular trichomes, whereas their overexpression increases it. While AaMYB1 belongs to a distinct lineage within the R2R3-MYB subfamily, both AaMIXTA1 and SlMX1 are classified as MIXTA-like genes (Yuan et al., 2023) [75] . Members of the HD-ZIP IV subfamily of transcription factors are known to play a crucial role in the differentiation of plant epidermal cells, contributing to cuticle biosynthesis as well as the patterning of trichomes and stomata (Zhang et al., 2019) [77] . Recent studies have shown that the HD-ZIP IV transcription factors AaHD1 and AaHD8 play a positive role in initiating glandular trichome development in Artemisia annua (Kovalchuk et al., 2019) [39] . Overexpression of either AaHD1 or AaHD8 results in an increase in glandular trichome density, while downregulation of both genes has the reverse effect (Fu et al., 2024) [21] . In tomatoes, AaHD8 acts upstream of AaHD1 to directly stimulate its expression (Hua, Chang, Xu, et al., 2021) [26, 71] . The closest homolog of AaHD8 in tomatoes is CUTIN DEFICIENT 2 (SlCD2) (Berhin et al., 2022) [4] . Due to a lossof-function mutation in SlCD2, the tomato sticky peel mutant has less glandular trichomes, especially type VI (Vendemiatti, 2020) [62] . Therefore, it seems that AaHD8/SlCD2 plays a similar role in the positive regulation of glandular trichome initiation in Artemisia annua and tomatoes. Another HD-ZIP IV transcription factor, WOOLLY (Wo), appears to be a crucial regulator of tomato glandular trichome initiation (Wu et al., 2023) [69] . Dominant point mutations in the C-terminus region of Wo induce the phenotypic of woolly mutants, which show noticeably greater trichome density in tomato plants (Yang et al., 2011) [73] . Given that type I glandular trichome density in tomatoes is lower in Wo-RNAi plants and higher in plants with dominant woolly mutations, the preliminary characterisation of Wo suggests that Wo stimulates type I glandular trichome initiation (Yu et al., 2024) [74] . However, a recent reanalysis of the phenotypic of woolly mutants shows that the type III and type V non-glandular trichome densities are larger and the type IV glandular trichome density is lower in tomato mature leaves (Gasparini et al., 2023) [22] . Two other transcription factors that are crucial for glandular trichome initiation but do not fall under the R2R3-MYB or HD-ZIP IV subfamilies have also been discovered in recent studies in tomatoes: The zinc-finger proteins MYELOCYTOMATOSIS-RELATED 1 (SlMYC1), a bHLH protein, and HAIR (SlH) C2H2 (Shvachko et al., 2020) [55] . RNAi-induced downregulation of SlMYC1 or missense mutations in SlH, respectively, reduce the density of type VI or type I glandular trichomes in tomatoes (Fonseca et al., 2022) [20] . Furthermore, SlH knockout produces a phenotype without hair, whereas myc1 knockout mutants in tomatoes lack type VI glandular trichomes (J. Xu et al., 2018) [72] . These results imply that SlMYC1 positively regulates the onset of type VI glandular trichomes in tomato plants and that SlH is an essential positive regulator of the commencement of all glandular trichome types (J. Xu et al., 2018) [72] . SlMYC1 is also a major regulator of later phases of tomato type VI glandular trichome morphogenesis, as evidenced by the interesting fact that SlMYC1 RNAi plants have smaller glands and shorter stalks in type VI glandular trichomes (J. Xu et al., 2018) [72] . [72] 2 Woolly (Wo) A homeodomain protein that mediates jasmonic acid signaling, influencing trichome initiation.

(Hua, Chang, Wu, et al., 2021) [27] 3 SlCycB2 A cyclin that interacts with Woolly to regulate type I trichome density. (Feng et al., 2021) [19] 4 HAIRPLUS (HAP) A gene involved in epigenomic modifications affecting glandular trichome density.

(Fonseca et al., 2022) [20] 5 SITRY Have negative impact on glandular trichome development in tomato plant.

(Tominaga-Wada et al., 2013) [59] Techniques that can apply to tomato plant to develop specific type of trichome A potent genome-editing technique called CRISPR-Cas9 can be used to create particular types of trichomes (Zlobin et al., 2020) [78] . CRISPR/Cas has dominated the area of genome editing in recent years due to its ease of use, adaptability, durability, and affordability (Wan et al., 2019) [64] . In order to address global climate change and other agricultural, environmental, and ecological concerns, its use in crop development is particularly important (M. D. Khan et al., 2023) [35] . Scientists have created a variety of CRISPR/Cas toolboxes that allow for precise genome changes, such as base editing, transcriptome regulation, epigenome editing, targeted mutagenesis at loci, and the exact replacement or tagging of genes and alleles in plants (Villiger et al., 2024) [63] . Two vectors, p2gR-TRI-A and p2gR-TRI-B, each carrying two gRNAs that targeted three genes linked to trichome formation, were used to alter tomatoes (Soda et al., 2018) [56] . Both vectors include the same gRNA (T2-ETC2), which targets ETC2 and maybe CPC, a far less desired target. The vectors also include distinct gRNAs (T1A-TC or T1B-TC) (Xing et al., 2014) [70] . In contrast to T1B-TC, T1A-TC's 18-bp target sequence is complimentary. Both T1A-TC and T1B-TC target two genes: TRY and CPC. While there are two mismatches between T1B-TC and CPC, there is only one between T1A-TC gRNA's 20-nt target and either TRY or CPC, and between T1B-TC and TRY. Approximately 70% of the T1 transgenic plants for p2gR-TRI-A had densely clustered trichomes, as expected for try cpc double or try cpc etc2 triple mutant plants (Kirik et al., 2004) [37] . Additionally, Crisper-cas 9 can control the synthesis of phytohormones that trigger the formation of particular trichomes (Rajput et al., 2021) [51] .

Using of Agrobacterium tumefaciens in producing glandular trichomes in tomato plants

To improve glandular trichome production and function, tomato plants are genetically modified using Agrobacterium tumefaciens (Kortbeek et al., 2016) [38] . The particular gene that produces glandular trichomes is included into A. tumefaciens' t-DNA (Chen et al., 2018) [8] . Genes involved in trichome initiation and development include WAX2, HD-Zip IV, and MIXTA-like (L. Wang et al., 2020) [66] . Under the guidance of an appropriate promoter, such as the 35S CaMV promoter for constitutive expression or glandular trichome-specific promoters like AAT1 or GPAT1, the chosen genes are cloned into a T-DNA section of a binary vector. Agrobacterium tumefaciens strains such as LBA4404 and GV3101 are exposed to the vector by heat shock or electroporation (Jeong et al., 2024) [30] . Agrobacterium suspension with the recombinant vector infects tomato explants (cotyledons, hypocotyls, or leaves) (Khamis et al., 2024) [34] . These genes are integrated into A. tumefaciens' t-DNA, which is then transferred to tomato plants. The bacteria target the DNA of the plants and produce glandular trichomes as a result (Brencic & Winans, 2005) [5] .

Conclusion

Trichomes are the hairlike structures that are formed on the stems, leaves, buds and other parts of the tomato plant. Mostly the trichomes are of two types glandular and non-glandular. These trichomes protects plant against insects and herbivore animal damage and protects from abiotic stresses and protects from transpiration. Plant trichome growth is controlled by environmental factors, hormones, regulatory genes, and noncoding RNA. Glandular trichomes plays a major role in protecting plant from herbivorous animals. The glandular trichome of type IV and type VI gives protection arthropod insects. These trichomes also protects plant from harmful UV-B rays. The glandular trichome development is regulated by 5 major genes like SlMYC1, Woolly (Wo), SlCycB2, HAIRPLUS (HAP), and SITRY. The techniques like Crisper cas9 and Agrobacterium tumefaciens are used to induce specific glandular trichomes in tomato plants. The Crisper cas9 uses gene editing, targeted mutagenesis at loci, and the exact replacement or tagging of genes and alleles in plants. By this we can produce glandular trichomes or other trichomes. The Agrobacterium tumefaciens use the technique it inserts specific gene. The specific gene inserts into t-DNA of A tumefaciens and these bacteria insert into plant's system the bacterium releases the specific gene into plants system and the glandular trichomes are formed. In this way glandular trichomes playa a major role in protection of plant from various stresses, and these mechanisms are used to produce various types of trichomes in plants.

References

1. Al-Khayri JM, Rashmi R, Toppo V, et al. Plant secondary metabolites: The weapons for biotic stress management. Metabolites. 2023;13(6):716. doi:10.3390/metabo13060716
2. Amr A, Raie W. Tomato components and quality parameters: A review. Jordan J Agric Sci. 2022;18(3):199220. doi:10.35516/jjas.v18i3.444
3. Bergau N, Bennewitz S, Syrowatka F, Hause G, Tissier A. The development of type VI glandular trichomes in the cultivated tomato Solanum lycopersicum and a related wild species S. habrochaites. BMC Plant Biol. 2015;15(1). doi:10.1186/s12870-015-0678-z
4. Berhin A, Nawrath C, Hachez C. Subtle interplay between trichome development and cuticle formation in plants. New Phytol. 2022;233(5):2036-2046. doi:10.1111/nph.17827
5. Brencic A, Winans SC. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev. 2005;69(1):155-194. doi:10.1128/mmbr.69.1.155-194.2005
6. Chaudhry S, Sidhu GPS. Climate change regulated abiotic stress mechanisms in plants: A comprehensive review. Plant Cell Rep. 2022;41(1). doi:10.1007/s00299-021-02759-5
7. Chen K, Dorlhac de Borne F, Sierro N, et al. Organization of the TC and TE cellular T-DNA regions in Nicotiana otophora and functional analysis of three diverged TE-6b genes. Plant J. 2018;94(2):274-287. doi:10.1111/tpj.13853
8. Collins EJ, Bowyer C, Tsouza A, Chopra M. Tomatoes: An extensive review of the associated health impacts of tomatoes and factors that can affect their cultivation. Biology. 2022;11(2):239. doi:10.3390/biology11020239
9. Dahl TW, Arens SKM. The impacts of land plant evolution on Earth's climate and oxygenation state -An interdisciplinary review. Chem Geol. 2020;547:119665. doi:10.1016/j.chemgeo.2020.119665
10. de Oliveira JRF, de Resende JTV, Filho RBL, et al. Tomato breeding for sustainable crop systems: High levels of zingiberene providing resistance to multiple arthropods. Horticulturae. 2020;6(2):34. doi:10.3390/horticulturae6020034
11. Deepa P. Trichomes: Targets for breeding biotic and abiotic stress tolerant plants. Bishen Singh Mahendra Pal Singh; 2024.
12. Despland E. Caterpillars cooperate to overcome plant glandular trichome defenses. Front Ecol Evol. 2019;7(JUL):232. doi:10.3389/fevo.2019.00232
13. Dhankhar R, Regmi K, Kawatra A, Gulati P. Trichomics: Trichomes as natural chemical factories. In: Phytochemical Genomics: Plant Metabolomics and Medicinal Plant Genomics. 2023:379-402. doi:10.1007/978-981-19-57796_15
14. Doroshkov AV, Konstantinov DK, Afonnikov DA, Gunbin KV. The evolution of gene regulatory networks controlling Arabidopsis thaliana L. trichome development. BMC Plant Biol. 2019;19. doi:10.1186/s12870-019-1640-2
15. Escobar-Bravo R, Ruijgrok J, Kim HK, et al. Light intensity-mediated induction of trichome-associated allelochemicals increases resistance against thrips in tomato. Plant Cell Physiol. 2018;59(12):2462-2475. doi:10.1093/pcp/pcy166
16. Ewas M, Harlina PW, Shahzad R, et al. Constitutive expression of SlMX1 gene improves fruit yield and quality, health-promoting compounds, fungal resistance, and delays ripening in transgenic tomato plants. J Plant Interact. 2022;17(1):517-536. doi:10.1080/17429145.2022.2066730
17. Fambrini M, Pugliesi C. The dynamic genetic-hormonal regulatory network controlling the trichome development in leaves. Plants. 2019;8(8):253. doi:10.3390/plants8080253
18. Feng Z, Bartholomew ES, Liu Z, Cui Y, Dong Y, Li S, et al. Glandular trichomes: New focus on horticultural crops. Hortic Res. 2021;8(1):5921. doi:10.1038/s41438-02100592-1
19. Fonseca R, Capel C, Yuste-Lisbona FJ, et al. Functional characterization of the tomato HAIRPLUS gene reveals the implication of the epigenome in the control of glandular trichome formation. Hortic Res. 2022;9:uhab015. doi:10.1093/hr/uhab015
20. Fu X, Zheng H, Wang Y, et al. AaABCG20 transporter involved in cutin and wax secretion affects the initiation and development of glandular trichomes in Artemisia annua. Plant Sci. 2024;339:111959. doi:10.1016/j.plantsci.2023.111959
21. Gasparini K, Gasparini J, Therezan R, et al. Natural genetic variation in the HAIRS ABSENT (H) gene increases typeVI glandular trichomes in both wild and domesticated tomatoes. J Plant Physiol. 2023;280:153859. doi:10.1016/j.jplph.2022.153859
22. Glas JJ, Schimmel BCJ, Alba JM, Escobar-Bravo R. Plant glandular trichomes as targets for breeding or engineering of resistance to herbivores. Int J Mol Sci. 2012;13(12):17077-17103. doi:10.3390/ijms131217077
23. Guo J, Yuan Y, Liu Z, Zhu J. Development and structure of internal glands and external glandular trichomes in Pogostemon cablin. PLoS One. 2013;8(10):77862. doi:10.1371/journal.pone.0077862
24. Han G, Li Y, Yang Z, Wang C, Zhang Y, Wang B. Molecular mechanisms of plant trichome development. Front Plant Sci. 2022;13:910228. doi:10.3389/fpls.2022.910228
25. Hua B, Chang J, Wu M, et al. Mediation of JA signalling in glandular trichomes by the woolly/SlMYC1 regulatory module improves pest resistance in tomato. Plant Biotechnol J. 2021;19(2):375-393. doi:10.1111/pbi.13473
26. Hua B, Chang J, Xu Z, et al. HOMEODOMAIN PROTEIN8 mediates jasmonate-triggered trichome elongation in tomato. New Phytol. 2021;230(3):1063-1077. doi:10.1111/nph.17216
27. Huegel CN. The Nature of Plants: An Introduction to How Plants Work. University Press of Florida; 2019.
28. Jeong JH, Jeon EY, Hwang MK, Song YJ, Kim JY. Development of super-infective ternary vector systems for enhancing the Agrobacterium-mediated plant transformation and genome editing efficiency. Hortic Res. 2024;11(9):uhea187. doi:10.1093/hr/uhae187
29. Karabourniotis G, Liakopoulos G, Nikolopoulos D, Bresta P. Protective and defensive roles of non-glandular trichomes against multiple stresses: structure-function coordination. J For Res. 2020;31(1):1-12. doi:10.1007/s11676-019-01034-4
30. Kariyat JK, R. Role of trichomes in plant stress biology. In: Evolutionary Ecology of Plant-Herbivore Interaction. 2020:1-376. doi:10.1007/978-3-030-46012-9
31. Kaur S, Khanal N, Dearth R, Kariyat R. Morphological characterization of intraspecific variation for trichome traits in tomato (Solanum lycopersicum). Bot Stud. 2023;64(1). doi:10.1186/s40529-023-00370-3
32. Khamis G, Chi J, Zhao Q. Establishment of an in vitro propagation, transformation, and gene editing system in tomato (Solanum lycopersicum). OBM Genet. 2024;8(2):2402244. doi:10.21926/obm.genet.2402244
33. Khan MD, Ahmad B, Ahmed SF. CRISPR-Cas genome editing in crops: A promising frontier for climate-smart agriculture. Phytopathogenomics and Disease Control. 2023;2(2):71-77. doi:10.22194/pdc/2.1022
34. Khan RA, Mohammad Hurrah IM, Muzafar S, Jan S, Abbas N. Transcriptional regulation of trichome development in plants: an overview. Proc Indian Natl Sci Acad. 2021;87(1):36-47. doi:10.1007/s43538-021-00017-6
35. Kortbeek RWJ, Xu J, Ramirez A, et al. Engineering of tomato glandular trichomes for the production of specialized metabolites. In: Methods in Enzymology. Academic Press; 2016. doi:10.1016/bs.mie.2016.02.014
36. Kovalchuk N, Wu W, Bazanova N, et al. Wheat woundingresponsive HD-Zip IV transcription factor GL7 is predominantly expressed in grain and activates genes encoding defensins. Plant Mol Biol. 2019;101(1-2):41-61. doi:10.1007/s11103-019-00889-9
37. Kundan M, Gani U, Nautiyal AK, Misra P. Molecular Biology of Glandular Trichomes and Their Functions in Environmental Stresses. In: Energy, Environment, and Sustainability. 2019. p. 365-93. Available from: https://doi.org/10.1007/978-981-15-0690-1_17
38. Li Y, Yang Y, Li L, Tang K, Hao X, Kai G. Advanced metabolic engineering strategies for increasing artemisinin yield in Artemisia annua L. Hortic Res. 2024;11(2). Available from: https://doi.org/10.1093/hr/uhad292
39. Lihavainen J, Ahonen V, Keski-Saari S, Sõber A, Oksanen E, Keinänen M. Low vapor pressure deficit reduces glandular trichome density and modifies the chemical composition of cuticular waxes in silver birch leaves. Tree Physiol. 2017;37(9):1166-81. Available from: https://doi.org/10.1093/treephys/tpx045
40. Liu Y, Jing SX, Luo SH, Li SH. Non-volatile natural products in plant glandular trichomes: Chemistry, biological activities and biosynthesis. Nat Prod Rep. 2019;36(4):62665. Available from: https://doi.org/10.1039/c8np00077h
41. Muravnik LE. The Structural Peculiarities of the Leaf Glandular Trichomes: A Review. In: Reference Series in Phytochemistry. 2020. p. 1-35. Available from: https://doi.org/10.1007/978-3-030-11253-0_3-1
42. Nandi D, Chakraborty A, Biswas T, Meher D, Singh AP. Role of trichomes in plant defence -A crop specific review. Crop Res. 2022;57(5 & 6):1-12. Available from: https://doi.org/10.31830/2454-1761.2022.895
43. Nowroz F, Hasanuzzaman M, Siddika A, Parvin K, Caparros PG, Nahar K, et al. Elevated tropospheric ozone and crop production: potential negative effects and plant defense mechanisms. Front Plant Sci. 2023;14. Available from: https://doi.org/10.3389/fpls.2023.1244515
44. Qiao Z, Song X, Kong Y, Shi S, Yan B, Egea-Cortines M, et al. Molecular mechanisms regulating ornamental traits and scent production in snapdragon (Antirrhinum majus L.). Hortic Adv. 2023;1(1). Available from: https://doi.org/10.1007/s44281-023-00019-y
45. Qin W, Xie L, Li Y, Liu H, Fu X, Chen T, et al. An R2R3MYB Transcription Factor Positively Regulates the Glandular Secretory Trichome Initiation in Artemisia annua L. Front Plant Sci. 2021;12. Available from: https://doi.org/10.3389/fpls.2021.657156
46. Rai K, Agrawal SB. Effects of elevated ultraviolet-B on the floral and leaf characteristics of a medicinal plant Wedelia chinensis (Osbeck) Merr. along with essential oil contents. Trop Ecol. 2023;64(2):307-23. Available from: https://doi.org/10.1007/s42965-022-00270-w
47. Rajput M, Choudhary K, Kumar M, Vivekanand V, Chawade A, Ortiz R, et al. RNA interference and CRISPR/Cas gene editing for crop improvement: Paradigm shift towards sustainable agriculture. Plants. 2021;10(9). Available from: https://doi.org/10.3390/plants10091914
48. Rakha M, Bouba N, Ramasamy S, Regnard JL, Hanson P. Evaluation of wild tomato accessions (Solanum spp.) for resistance to two-spotted spider mite (Tetranychus urticae Koch) based on trichome type and acylsugar content. Genet Resour Crop Evol. 2017;64(5):1011-22. Available from: https://doi.org/10.1007/s10722-016-0421-0
49. Savi PJ. Resistant genotypes, biological control, and selective pesticides for the integrated management of Tetranychus evansi (Acari: Tetranychidae) on tomato. Universidade Estadual Paulista Faculdade de Ciências Agrárias e Veterinárias. 2022.
50. Schuurink R, Tissier A. Glandular trichomes: micro-organs with model status? New Phytol. 2020;225(6):2251-66. Available from: https://doi.org/10.1111/nph.16283
51. Shvachko NA, Semilet TV, Tikhonova NG. Trichomes of Higher Plants: Homologous Series in Hereditary Variability and Molecular Genetic Mechanisms. Russ J Genet. 2020;56(11):1359-70. Available from: https://doi.org/10.1134/S1022795420110083
52. Soda N, Verma L, Giri J. CRISPR-Cas9 based plant genome editing: Significance, opportunities and recent advances. Plant Physiol Biochem. 2018;131:2-11. Available from: https://doi.org/10.1016/j.plaphy.2017.10.024
53. Tabary L, Navajas M, Tixier M-S, Navia D. Tomato trichomes: trade-off between plant defenses against pests and benefits for biological control agents. 2024. Available from: https://doi.org/10.24349/ej2w-b311
54. Tian N, Liu F, Wang P, Zhang X, Li X, Wu G. The molecular basis of glandular trichome development and secondary metabolism in plants. Plant Gene. 2017;12:1-12. Available from: https://doi.org/10.1016/j.plgene.2017.05.010
55. Tominaga-Wada R, Nukumizu Y, Wada T. Tomato (Solanum lycopersicum) homologs of TRIPTYCHON (SLTRY) and GLABRA3 (SLGL3) are involved in anthocyanin accumulation. Plant Signal Behav. 2013;8(7). Available from: https://doi.org/10.4161/psb.24575
56. Tsugawa H, Rai A, Saito K, Nakabayashi R. Metabolomics and complementary techniques to investigate the plant phytochemical cosmos. Nat Prod Rep. 2021;38(10):172959. Available from: https://doi.org/10.1039/d1np00014d
57. Uzelac B, Stojičić D, Budimir S. Glandular trichomes on the leaves of Nicotiana tabacum: Morphology, developmental ultrastructure, and secondary metabolites. In: Reference Series in Phytochemistry. 2019. Available from: https://doi.org/10.1007/978-3-030-11253-0_1-1
58. Vendemiatti E. Genetic and molecular characterization of type-IV glandular trichome development in tomato (Solanum lycopersicum cv. Micro-Tom) and its participation in arthropod resistance. Piracicaba; 2020.
59. Villiger L, Joung J, Koblan L, Weissman J, Abudayyeh OO, Gootenberg JS. CRISPR technologies for genome, epigenome and transcriptome editing. Nat Rev Mol Cell Biol. 2024;25(6):464-87. Available from: https://doi.org/10.1038/s41580-023-00697-6
60. Wan T, Niu D, Wu C, Xu FJ, Church G, Ping Y. Material solutions for delivery of CRISPR/Cas-based genome editing tools: Current status and future outlook. Mater Today. 2019;26(June):40-66. Available from: https://doi.org/10.1016/j.mattod.2018.12.003
61. Wang F, Wang F, Virginia W. Identification of sesquiterpenes in wild tomato accessions with activities against the potato aphid and their tissue-specific engineering in cultivated tomato. 2022.
62. Wang L, Xue W, Li X, Li J, Wu J, Xie L, et al. EgMIXTA1, a MYB-type transcription factor, promotes cuticular wax formation in Eustoma grandiflorum leaves. Front Plant Sci. 2020;11. Available from: https://doi.org/10.3389/fpls.2020.524947
63. Wang X, Shen C, Meng P, Tan G, Lv L. Analysis and review of trichomes in plants. BMC Plant Biol. 2021;21(1):327. Available from: https://doi.org/10.1186/s12870-021-02840-x
64. Watts S, Kariyat R. Are epicuticular waxes a surface defense comparable to trichomes? A test using two Solanum species and a specialist herbivore. Botany. 2022;101(1):1523. Available from: https://doi.org/10.1139/cjb-2021-0206
65. Wu M, Chang J, Han X, Shen J, Yang L, Hu SB, et al. A HD-ZIP transcription factor specifies fates of multicellular trichomes via dosage-dependent mechanisms in tomato. Dev Cell. 2023;58(4):278-88. Available from: https://doi.org/10.1016/j.devcel.2023.01.009
66. Xing HL, Dong L, Wang ZP, Zhang HY, Han CY, Liu B, et al. A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biol. 2014;14(1):327. Available from: https://doi.org/10.1186/s12870-014-0327-y
67. Xu B, Taylor L, Pucker B, Feng T, Glover BJ, Brockington SF. The land plant-specific MIXTA-MYB lineage is implicated in the early evolution of the plant cuticle and the colonization of land. New Phytol. 2021;229(4):2324-38. Available from: https://doi.org/10.1111/nph.16997
68. Xu J, Van Herwijnen ZO, Dräger DB, Sui C, Haring MA, Schuurink RC. SlMYC1 regulates type VI glandular trichome formation and terpene biosynthesis in tomato glandular cells. Plant Cell. 2018;30(12):2988-3005. Available from: https://doi.org/10.1105/tpc.18.00571
69. Yang C, Li H, Zhang J, Luo Z, Gong P, Zhang C, et al. A regulatory gene induces trichome formation and embryo lethality in tomato. Proc Natl Acad Sci U S A. 2011;108(29):11836-41. Available from: https://doi.org/10.1073/pnas.1100532108
70. Yu L, Zhang Y, Ding Q, Wang H, Meng X, Fan H, et al. The SlMYC1-TOR module regulates trichome formation and terpene biosynthesis in tomatoes (Solanum lycopersicum L.). J Plant Growth Regul. 2024;43(9):328294. Available from: https://doi.org/10.1007/s00344-02411292-0
71. Yuan Y, Wang Q, Tong B, Liu D, Liu H, Yan Q, et al. Morphological studies of developing glandular trichomes and a novel HD-ZIP gene LjROC3 increasing glandular trichome density on leaves in honeysuckle (Lonicera japonica). Ind Crops Prod. 2023;198(March):116696. Available from: https://doi.org/10.1016/j.indcrop.2023.116696
72. Zhang H, Liu P, Wang B, Yuan F. The roles of trichome development genes in stress resistance. Plant Growth Regul. 2021;95(2):137-48. Available from: https://doi.org/10.1007/s10725-021-00733-5
73. Zhang H, Ma X, Li W, Niu D, Wang Z, Yan X, et al. Genome-wide characterization of NtHD-ZIP IV: different roles in abiotic stress response and glandular trichome induction. BMC Plant Biol. 2019;19(1):444. Available from: https://doi.org/10.1186/s12870-019-2023-4
74. Zlobin NE, Lebedeva MV, Taranov VV. CRISPR/Cas9 genome editing through in planta transformation. Crit Rev Biotechnol. 2020;40(2):153-68. Available from: https://doi.org/10.1080/07388551.2019.1709795