Secretome-Derived Cultured Cell System: Overview Towards Extracellular Protein Characterization and Biotechnological Applications
PDF

Keywords

Secretome
cell cultures
extracellular proteins
embryogenic suspensions

How to Cite

Anis Ben-Amar. (2021). Secretome-Derived Cultured Cell System: Overview Towards Extracellular Protein Characterization and Biotechnological Applications. Journal of Basic & Applied Sciences, 17, 13–24. https://doi.org/10.29169/1927-5129.2021.17.02

Abstract

Secretome released by plant cells into the extracellular space, play crucial roles during development, embryonic potential acquisition, nutrient backing and stress acclimation. The dynamic nature of the extracellular proteome presents the challenge of identifying an array of extracellular proteins involved in the regulation of somatic embryogenesis in embryogenic suspension cultures. Extracellular proteins produced by cell cultures are perceived here as a central node of overlapping regulator factor network of totipotent somatic embryo developmental process. This paper reviews in a morphogenetic aspect the biological processes associated with extracellular protein-derived plant cultured cells and explores their prospective biotechnological applications in laboratories and biofactories retated to cell signaling and metabolism, developmental process, and biotic / abiotic stress tolerance. The role of extracellular proteins in acquisition and maintenance of embryonic potential and their relevance are especially emphasized.

https://doi.org/10.29169/1927-5129.2021.17.02
PDF

References

Quiroz-Figueroa F, Mendez-Zeel M, Sanchez-Teyer F, Rojas-Herrera R, Loyola-Vargas VM. Differential gene expression in embryogenic and non-embryogenic clusters from cell suspension cultures of Coffea arabica. J Plant Physiol 2002; 159(11): 1267-1270. https://doi.org/10.1078/0176-1617-00878

Wen L, Li W, Parris S, West M, Lawson J, Smarthers M, Li Z, Jones D, Jin S, Saski CA. Transcriptomic profiles of non-embryogenic and embryogenic callus cells in a highly regenerative upland cotton line Gossypium hirsutum L. BMC Dev Biol 2020; 20: 25. https://doi.org/10.1186/s12861-020-00230-4

Yang XY, Zhang XL. Regulation of somatic embryogenesis in higher plants. Crit Rev Plant Sci 2010; 29(1): 36-57. https://doi.org/10.1080/07352680903436291

Feher A, Pasternak T, Dudits D. Transition of somatic plant cells to embryogenic state. Plant Cell Tiss Org Cult 2003; 74(3): 201-228. https://doi.org/10.1023/A:1024033216561

Ibanez S, Carneros E, Testillano PS, Pérez-Pérez JM. Advances in plant regeneration: Shake, rattle and roll. Plants 2020; 9: 897. https://doi.org/10.3390/plants9070897

Soriano M, Li H, Boutilier K. Microspore embryogenesis: establishment of embryo identity and pattern in culture. Plant Reprod 2013; 26(3): 181-196. https://doi.org/10.1007/s00497-013-0226-7

Gambino G, Ruffa P, Gribaudo I, Vallania R. Somatic embryogenesis from whole flowers, anthers and ovaries of grapevine (Vitis spp.). Plant Cell Tiss Org Cult 2007; 90(1): 79-83. https://doi.org/10.1007/s11240-007-9256-x

Bouamama B, Ben Salem-Fnayou A, Zoghlami N, Zemni H, Mliki A, Ghorbel A. Somatic embryogenesis and plantlet regeneration from immature anthers of Opuntia ficus-indica. J Hort Sci Biotechnol 2011; 86(4): 313-318. https://doi.org/10.1080/14620316.2011.11512766

Sauer U, Wilhelm E. Somatic embryogenesis from ovaries, developing ovules and immature zygotic embryos and improved embryo development from Castanea sativa. Biol Plant 2005; 49: 1-6. https://doi.org/10.1007/s10535-005-1006-5

Pérez-Pérez Y, El-Tantawy A-A, Solís MT, Risueño MC, Testillano PS. Stress-induced microspore embryogenesis requires endogenous auxin synthesis and polar transport in barley. Front Plant Sci 2019; 10: 1200. https://doi.org/10.3389/fpls.2019.01200

Pires R, Cardoso H, Ribeiro A, Peixe A, Cordeiro A. Somatic embryogenesis from mature embryos of Olea europea L. cv. "Galega Vulgar" and long-term management of calli morphogenic capacity. Plants 2020; 9: 758. https://doi.org/10.3390/plants9060758

Purohit S, Kothari SL. Direct somatic embryogenesis from cotyledon and cotyledonary node explants in bishop's weed Trachyspermum ammi (L.) sprague. In Vitro Cell Dev Biol-Plant 2007; 43: 154-158. https://doi.org/10.1007/s11627-007-9039-4

Fei Y, Wang LX, Fang ZW, Liu ZX. Somatic embryogenesis and plant regeneration from cotyledon and hypocotyl explants of Fagopyru esculentum Moench lpls mutant. Agronomy 2019; 9: 768. https://doi.org/10.3390/agronomy9110768

Capelo AM, Silva S, Brito G, Santos C. Somatic embryogenesis induction in leaves and petioles of mature wild olive. Plant Cell Tiss Org Cult 2010; 103: 237-242. https://doi.org/10.1007/s11240-010-9773-x

Konar S, Karmakar J, Ray A, Adhikari S, Bandyopadhyay TK. Regeneration of plantlets through somatic embryo-genesis from root derived calli of Hibiscus sabdariffa L. (Roselle) and assessment of genetic stability by flow cyto-metry and ISSR analysis. PLoS ONE 2018; 13(8): e0202324. https://doi.org/10.1371/journal.pone.0202324

Bhusare BP, John CK, Bhatt VP, Nikam TD. Induction of somatic embryogenesis in leaf and root explants of Digitalis lanata Ehrh.: Direct and indirect method. South Afr J Bot 2020; 130: 356-365. https://doi.org/10.1016/j.sajb.2020.01.012

Kadokura S, Sugimoto K, Tarr P, Suzuki T, Matsunaga S. Characterization of somatic embryogenesis initiated from the Arabidopsis shoot apex. Dev Biol 2018; 442(1): 13-27. https://doi.org/10.1016/j.ydbio.2018.04.023

Shen HJ, Chen JT, Chung HH, Chang WC. Plant regeneration via direct somatic embryogenesis from leaf explants of Tolumnia Louise Elmore Elsa. Bot Stud 2018; 59: 4. https://doi.org/10.1186/s40529-018-0220-3

Zimmerman JL. Somatic embryogenesis: A model for early development in higher plants. Plant Cell 1993; 5: 1411-1423. https://doi.org/10.2307/3869792

Patidar SL, Tripathi MK, Tiwari G, Patel RP, Ahuja A. Standardization of an efficient and reproducible embryogenic suspension culture protocol for production of secondary metabolites in Plumbago zeylanica Linn. Eco Env Conserv 2017; 23(1): 361-372.

Haida Z, Syahida A, Ariff SM, Maziah M, Hakiman M. Factors affecting cell biomass and flavonoid production of Ficus deltoidea var. kunstleri in cell suspension culture system. Sci Rep 2019; 9: 9533. https://doi.org/10.1038/s41598-019-46042-w

Tomiczak K, Mikuła A, Niedziela A, Wójcik-Lewandowska A, Domzalska L, Rybczynski JJ. Somatic embryogenesis in the family Gentianaceae and its biotechnological application. Front Plant Sci 2019; 10: 762. https://doi.org/10.3389/fpls.2019.00762

Marchev AS, Yordanova ZP, Georgiev MI. Green cell factories for advanced production of plant secondary metabolites. Crit Rev Biotechnol 2020; 40(4): 443-458. https://doi.org/10.1080/07388551.2020.1731414

Matsubayashi Y, Sakagami Y. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 1996; 93(15): 7623-7627. https://doi.org/10.1073/pnas.93.15.7623

Matthys-Rochon E. Secreted molecules and their role in embryo formation in plants: a mini-review. Acta Biol Cracov - Botanica 2005; 47(1): 23-29.

De Vries SC, Booij H, Meyerink P, Huisman G, Wilde HD, Thomas TL, Van Kammen AB. Acquisition of embryogenic potential in carrot cell-suspension cultures. Planta 1988; 176: 196-204. https://doi.org/10.1007/BF00392445

Coutos-Thévenot P, Goebel-Tourand I, Mauro MC, Boulay M, Deloire A, Guern J. Somatic embryogenesis from grapevine cells. I- Improvement of embryo development by changes in culture conditions. Plant Cell Tiss Org Cult 1992-a; 29: 125-133. https://doi.org/10.1007/BF00033617

Ben-Amar A, Cobanov P, Boonrod K, Bouzid S, Ghorbel A, Krczal G, Reustle G. Efficient procedure for grape embryogenic suspensions establishment and plant regeneration: role of conditioned medium in cell proliferation. Plant Cell Rep 2007; 26: 1139-1147. https://doi.org/10.1007/s00299-007-0341-8

Von Arnold S, Egertsdotter U, Mo LH. Importance of extracellular proteins for somatic embryogenesis in Picea abies. Curr Issue Plant Mol Cell Biol 1995; 22: 389-392. https://doi.org/10.1007/978-94-011-0307-7_54

Ben-Amar A, Reustle G. Extracellular protein-induced plant cell proliferation. In: Zhang C., Zeng X. Eds. Cell Proliferation: Process, Regulation and Disorders. New York: Nova Science Publisher 2013; pp. 65-80. ISBN: 978-1-62417-352-3. https://doi.org/10.1007/s10535-010-0055-6

Ben-Amar A, Cobanov P, Ghorbel A, Mliki A, Reustle G. Involvement of Arabinogalactan proteins in the control of cell proliferation of zucchini squash (Cucurbita pepo L.) suspension cultures. Biol Plant 2010; 54(2): 321-324.

Coutos-Thévenot P, Maes O, Jouenne T, Mauro MC, Jouanneau JP, Boulay M, Deloire A, Guern J. Extracellular protein patterns of grapevine cell suspensions in embryogenic and non-embryogenic situations. Plant Sci 1992-b; 86(2): 137-145. https://doi.org/10.1016/0168-9452(92)90159-J

Van Engelen A, Sterk P, Booij H, Cordewener JHG, Rook W, Van Kammen A, De Vries SC. Heterogeneity and cell type-specific localization of a cell wall glycoprotein from carrot suspension cells. Plant Physiol 1991; 96: 705-712. https://doi.org/10.1104/pp.96.3.705

Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC. Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 1991; 3: 907-921. https://doi.org/10.1105/tpc.3.9.907

De Jong AJ, Cordewener J, Schiavo L, Terzi M, Vanderkerckhove J, Van Kammen A, De Vries SC. A carrot somatic embryo mutant is rescued by chitinase. Plant Cell 1992; 4: 425-433. https://doi.org/10.1105/tpc.4.4.425

Van Hengel AJ, Guzzo F, Van Kammen A, De Vries SC. Expression pattern of the carrot EP3 endochitinase genes in suspension cultures and in developing seeds. Plant Physiol 1998; 117: 43-53. https://doi.org/10.1104/pp.117.1.43

Mukul-Lopez HG, De-la-Pena C, Galaz-Avalos RM, Loyola-Vargas VM. Evaluation of the extracellular proteome profile during the somatic embryogenesis process of Coffea spp. J Mex Chem Soc 2012; 56(1): 72-79. https://doi.org/10.29356/jmcs.v56i1.278

Bhuyan S, Bordoloi R. Expression of extracellular proteins in somatic embryogenesis of plants. Int J Pharmac Sci Inv 2019; 8(1): 1-7.

Ohmiya Y, Samejima M, Shiroishi M, Amano Y, Kanda T, Sakai F, Hayashi T. Evidence that endo-1,4-β-glucanases act on cellulose in suspension-cultured poplar cells. Plant J 2000; 24(2): 147-158. https://doi.org/10.1046/j.1365-313x.2000.00860.x

Edington BV, Lamb CJ, Dixon RA. cDNA cloning and characterization of a putative 1,3-β-D-glucanase transcript induced by fungal elicitor in bean cell suspension cultures. Plant Mol Biol 1991; 16: 81-94. https://doi.org/10.1007/BF00017919

Zhong R, Kays SJ, Schroeder BP, Ye ZH. Mutation of a chitinase-like gene causes ectopic deposition of lignin, aberrant cell shapes, and overproduction of ethylene. Plant Cell 2002; 14: 165-179. https://doi.org/10.1105/tpc.010278

Van Hengel A, Tadesse Z, Immerzeel P, Schols H, Van Kammen A, De Vries SC. N-Acetylglucosamine and glucosamine-containing Arabinogalactan proteins control somatic embryogenesis. Plant Physiol 2001; 125(4): 1881-1890. https://doi.org/10.1104/pp.125.4.1880

Von Arnold S, Bozhkov P, Clapham D, Dyachok J, Filonova L, Hogberg KA, Ingouff M, Wiweger M. Progagation of Norway spruce via somatic embryogenesis. Plant Cell Tiss Org Cult 2005; 81: 323-329. https://doi.org/10.1007/s11240-004-6662-1

Showalter AM, Basu D. Glycosylation of arabinogalactan-proteins essential for development in Arabidopsis. Com Integr Biol 2016-a; 9(3): e1177687. https://doi.org/10.1080/19420889.2016.1177687

Showalter AM, Basu D. Extensins and arabinogalactan proteins biosynthesis: glycosyl-transferases, research challenges, and biosensors. Front Plant Sci 2016-b; 7: 814. https://doi.org/10.3389/fpls.2016.00814

Van Hengel A, Van Kammen A, De Vries SC. A relationship between seed development, Arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiol Plant 2002; 114(4): 637-644. https://doi.org/10.1034/j.1399-3054.2002.1140418.x

Knox JP. The use of antibodies to study the architecture and developmental regulation of plant cell walls. Int Rev Cytol 1997; 171: 79–120. https://doi.org/10.1016/S0074-7696(08)62586-3

Yariv J, Rapport MM, Graf L. The interaction of glycosides and saccharides with antibody to the corresponding phenylazo-glycosides. Biochem J 1962; 85: 383-388. https://doi.org/10.1042/bj0850383

McCabe PF, Valentine TA, Forsberg LS, Pennell RI. Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 1997; 9: 225- 241. https://doi.org/10.2307/3870581

Borderies G, Le Bechec M, Rossignol M, Lafitte C, Le Deunff E, Beckert M, Dumas C, Matthys–Rochon E. Characterization of proteins secreted during maize microspore culture: arabinogalactan proteins (AGPs) stimulate embryo development. Eur J Cell Biol 2004; 83: 205-212. https://doi.org/10.1078/0171-9335-00378

Paire A, Devaux P, Lafitte C, Dumas C, Matthys-Rochon E. Proteins produced by barley microspores and their derived androgenic structures promote in vitro zygotic maize embryo formation. Plant Cell Tiss Org Cult 2003; 73: 167–176. https://doi.org/10.1023/A:1022805623167

Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y. Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Mol Biol 2006; 60: 167–183. https://doi.org/10.1007/s11103-005-3381-x

Chen Y, Xu X, Liu Z, Zhang Z, Xu-Han X, Lin Y, Lai Z. Global scale transcriptome analysis reveals differentially expressed genes involve in early somatic embryogenesis in Dimocarpus longan Lour. BMC Genomics 2020; 21: 4. https://doi.org/10.1186/s12864-019-6393-7

Kader JC. Lipid transfer proteins: a puzzling family of plant proteins. Trends Plant Sci. 1997; 2(2): 66-70. https://doi.org/10.1016/S1360-1385(97)82565-4

Garcia-Olmedo F, Molina A, Segura A, Moreno M. The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol 1995; 3(2): 72-74. https://doi.org/10.1016/S0966-842X(00)88879-4

Kristensen AK, Brunstedt J, Nielson KK, Roepstorff P, Millelsen JD. Characterization of a new antifungal non specific lipid transfer protein (nsLTP) from sugar beet leaves. Plant Sci 2000; 155: 31-40. https://doi.org/10.1016/S0168-9452(00)00190-4

Hincha DK, Neukamm B, Sror HAM, Sieg F, Weckwarth W, Ruckels M, Lullien-Pellerin V, Schroder W, Schmitt JM. Cabbage cryoprotectin is a member of nonspecific plant lipid transfer protein gene family. Plant Physiol 2001; 125: 835-846. https://doi.org/10.1104/pp.125.2.835

Trevino MB, O'Connell MA. Three drought-responsive members of the nonspecific lipid-transfer protein gene family in Lycopersicum pennellii show different developmental patterns of expression. Plant Physiol 1998; 116: 1461-1468. https://doi.org/10.1104/pp.116.4.1461

Finkina EI, Melnikova DN, Bogdanov IV, Ovchinnikova TV. Lipid transfer proteins as components of the plant innate immune system: structure, functions, and applications. Acta Naturae 2016; 8(2): 47–61. https://doi.org/10.32607/20758251-2016-8-2-47-61

Malinowski R, Filipecki M. The role of cell wall in plant embryogenesis. Cell Mol Biol Lett 2002; 7: 1137–1151.

Smertenko A, Bozhkov PV. Somatic embryogenesis: life and death processes during apical-basal patterning. J Exp Bot 2014; 65(5): 1343-1360. https://doi.org/10.1093/jxb/eru005

Murshid A, Thriault J, Gong J, Calderwood SK. Receptors for extracellular heat shock proteins. Methods Mol Biol 2011; 787: 289-302. https://doi.org/10.1007/978-1-61779-295-3_22

Ahuja I, De Vos RCH, Bones AM, Hall RD. Plant molecular stress responses face climate change. Trends Plant Sci 2010; 15: 664-674. https://doi.org/10.1016/j.tplants.2010.08.002

Haq S, Khan A, Ali M, Khattak AM, GAi WX, Zhang HX, Wei AM, Gong ZH. Heat shock proteins: Dynamic biomolecules to counter plant biotic and abiotic stresses. Int J Mol Sci 2019; 20: 5321. https://doi.org/10.3390/ijms20215321

Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH. The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Front Plant Sci 2016; 7: 114. https://doi.org/10.3389/fpls.2016.00114

Liu HT, Li B, Shang ZL, Li XZ, Mu RL, Sun DY, Zhou RG. Ca2+ and AtCaM3 are involved in the expression of heat shock protein gene in Arabidopsis. Plant Cell Env 2003; 28(10): 1276-1284. https://doi.org/10.1111/j.1365-3040.2005.01365.x

Li B, Liu HT, Sun DY, Zhou RG. Ca2+ and calmodulin mo-dulate DNA-binding activity of maize heat shock transcription factor in vitro. Plant Cell Physiol 2004; 45: 627-634. https://doi.org/10.1093/pcp/pch074

Liu HT, Li B, Sun DY, Zhou RG. Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 2005; 132: 1186-1195. https://doi.org/10.1104/pp.102.018564

Mita G, Nocco G, Leuci C, Greco V, Rampino P, Perrotta C. Secreted heat shock proteins in sunflower suspension cell cultures. Plant Cell Rep 1997; 16: 792-796. https://doi.org/10.1007/s002990050322

Ngcala MG, Goche T, Brown AP, Chivasa S, Ngara R. Heat stress triggers differential protein accumulation in the extracellular matrix of Sorghum cell suspension cultures. Proteomes 2020; 8: 29. https://doi.org/10.3390/proteomes8040029

Pedrosa AM, Martins CPS, Conçales LP, Costa MGC. Late embryogenesis abundant (LEA) constitutes a large and diverse family of proteins involved in development and abiotic stress responses in sweet orange (Citrus sinensis L. Osb.). PloS One 2015; 10(12): e0145785. https://doi.org/10.1371/journal.pone.0145785

Hundertmark M, Hincha DK. LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 2008; 9: 118. https://doi.org/10.1186/1471-2164-9-118

Tolleter D, Hincha DK, Macherel D. A mitochondrial late embryogenesis abundant protein stabilizes model membranes in the dry state. Biochim Bioph Acta-Biomembr 2010; 1798(10): 1926-1933. https://doi.org/10.1016/j.bbamem.2010.06.029

Bisseling T. The role of plant peptides in intercellular signaling. Curr Opin Plant Biol 1999; 2: 365-368. https://doi.org/10.1016/S1369-5266(99)00006-0

Hanai H, Matsuno T, Yamamoto M, Matsubayasho Y, Koboyashi T, Kamada H, Sakagami Y. A secreted peptide growth factor, phytosulfokine, acting as stimulatory factor of carrot somatic embryo formation. Plant Cell Physiol 2000; 41(1): 27-32. https://doi.org/10.1093/pcp/41.1.27

Igasaki T, Akasho N, Ujino-Ihara T, Matsubayashi Y, Sakagami Y, Shinohara K. Phytosulfokine stimulates somatic embryogenesis in Cryptomeria japonica. Plant Cell Physiol 2003; 44(12): 1412-1416. https://doi.org/10.1093/pcp/pcg161

Motose H, Iwamoto K, Endo S, Demura T, Sakagami Y, Matsubayashi Y, Moore KL, Fukuda H. Involvement of phytosulfokine in the attenuation of stress response during the transdifferentiation of zinnia mesophyll cellls into tracheary elements. Plant Physiol 2009; 150: 437-447. https://doi.org/10.1104/pp.109.135954

Kielkowska A, Adamus A. Peptide growth factor phytosulfokine -α stimulates cell divisions and enhances regeneration from B.oleracea var. capitata L. protoplast culture. J Plant Growth Regul 2019; 38: 931-944. https://doi.org/10.1007/s00344-018-9903-y

Stührwohldt N, Bühler E, Sauter M, Schaller A. Precursor processing by SBT3.8 and phytosulfokine signaling contribute to drought stress tolerance in Arabidopsis. J Exp Bot 2020. https://doi.org/10.1093/jxb/erab017

Bernier F, Berna A. Germins and germin-like proteins: Plant do-allproteins. But what do they do exactly? Plant Physiol Biochem 2001; 39: 545-554. https://doi.org/10.1016/S0981-9428(01)01285-2

Domon JM, Neutelings G, Roger D, Daid A, David H. Three glycosylated polypeptides secreted by several embryogenic cell cultures of pine show highly specific serological affinity to antibodies directed against the wheat germin apoprotein monomer. Plant Physiol 1995; 108: 141-148. https://doi.org/10.1104/pp.108.1.141

Çaliskan M, Turet M, Cuming AC. Formation of wheat (Triticum aestivum L.) embryogenic callus involves peroxide-generating germin-like oxalate oxidase. Planta 2004; 219: 132-140. https://doi.org/10.1007/s00425-003-1199-9

Ngara R, Ndimba B. Mapping and characterization of the sorghum cell culture secretome. Afr J Biotechnol 2011; 10(2): 253-266.

Koltunow AM, Hidaka T, Robinson SP. Polyembryony in Citrus: Accumulation of seed storage proteins in seeds and in embryos cultured in vitro. Plant Physiol 1996; 110: 599-609. https://doi.org/10.1104/pp.110.2.599

Barondes SH. Soluble lectins: a new class of extracellular proteins. Science 1984; 223(4642): 1259-1264. https://doi.org/10.1126/science.6367039

Bellande K, Bono J-J, Savelli B, Jamet E, Canut H. Plant lectins and lectin receptor-like kinases: how do they sense the outside? Int J Mol Sci 2017; 18(6): 1164. https://doi.org/10.3390/ijms18061164

Pinedo M, Regente M, Elizalde M, Quiroga Y, Pagnussat L, Jorrin-Novo J, Maldonado-Alconada AM, de la Canal L. Extracellular sunflower proteins: Evidence on non-classical secretion of a jacalin-related lectin. Prot Pept Lett 2011; 19(3): 270-276. https://doi.org/10.2174/092986612799363163

Muramoto K. Lectins as bioactive proteins in foods and feeds. Food Sci Technol Res 2017; 23(4): 487-494. https://doi.org/10.3136/fstr.23.487

Clement F, Pramod SN, Yeldur P, Venkatesh YP. Identify of the immunomodulatory proteins from garlic (Allium sativum) with the major garlic lectins or agglutins. Int Immunpharmacol 2010; 10: 316-324. https://doi.org/10.1016/j.intimp.2009.12.002

Fu LL, Zhou CC, Yao S, Yu JY, Liu B, Bao JK. Plant lectins: Targeting programmed cell death pathways as antitumor agents. Int J Biochem Cell Biol 2011; 43: 1442-1449. https://doi.org/10.1016/j.biocel.2011.07.004

Dias RO, Machado LS, Migliolo L, Franco OL. Insights into animal and plant lectins with antimicrobial activities. Molecules 2015; 20: 519-541. https://doi.org/10.3390/molecules20010519

Egertsdotter U, Von Arnold S. Importance of arabinogalactan proteins for development of somatic embryos of Norway spruce (Picea abies). Physiol Plant 1998; 93: 334-345. https://doi.org/10.1111/j.1399-3054.1995.tb02237.x

Cao S, Wang Y, Li Z, Shi W, Gao F, Zhou Y, Zhang G, Feng J. Genome-wide identification and expression analyses of the chitinases under cold and osmotic stress in Ammopiptanthus nanus. Genes 2019; 10: 472. https://doi.org/10.3390/genes10060472

Oyeleye A, Normi YM. Chitinase: diversity, limitations and trends in engineering for suitable applications. Biosci Rep 2018; 38: BSR2018032300. https://doi.org/10.1042/BSR20180323

Žiarovská J, Zamiešková L, Bilcíková J, Fialková V, Sabo J, Kunová S, Kacániová M. Expression of specific class I chitinase mRNA levels in different grape varieties and their antimicrobial activity. Agronomie 2020; 10: 1176. https://doi.org/10.3390/agronomy10081176

Shukla M, Jalil SU. Endochitinase: engineered resistance against fungal plant pathogens. Res Env Life Sci 2014; 7(3): 137-142.

Jabeen N, Chaudhary Z, Gulfraz M, Rashid H, Mirza B. Expression of rice chitinase gene in genetically engineered tomato confers enhanced resistance to Fusarium wilt and early blight. Plant Pathol J 2015; 31(3): 252-258. https://doi.org/10.5423/PPJ.OA.03.2015.0026

Schultz C, Gilson P, Oxley D, Youl J, Bacic A. GPI-anchors on arabinogalactan-proteins: implications for signaling in plants. Trends Plant Sci 1998; 3: 426-431. https://doi.org/10.1016/S1360-1385(98)01328-4

Showalter AM. Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 2001; 58: 1399–1417. https://doi.org/10.1007/PL00000784

Lee KJD, Sakata Y, Mau SL, Pettolino F, Bacic A, Quatrano RS, Knight CD, Knox JP. Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens. Plant Cell 2005; 17: 3051-3065. https://doi.org/10.1105/tpc.105.034413

Ben-Amar A, Daldoul S, Allel D, Reustle G, Mliki A. Reliable encapsulation-based cryopreservation protocol for safe storage and recovery of grapevine embryogenic cell cultures. Sci Horticult 2013; 157: 32-38. https://doi.org/10.1016/j.scienta.2013.04.005

Lamport DT, Kieliszewski MJ, Showalter AM. Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyze AGP function. New Phytol 2006; 169: 479-492. https://doi.org/10.1111/j.1469-8137.2005.01591.x

Mareri L, Romi M, Cai G. Arabinogalactan proteins; actors or spectators during abiotic and biotic stress in plants? Plant Biosyst 2018: 153(1); 173-185. https://doi.org/10.1080/11263504.2018.1473525

Li X, Zhang H, Jin Q, Cai Z. Contribution of arabinogalactan protein to the stabilization of single-walled carbon nanotubes in aqueous solution of gum arabic. Food Hydrocoll 2018; 78: 55-61. https://doi.org/10.1016/j.foodhyd.2017.08.013

Ellis M, Egelund J, Schultz CJ, Bacic A. Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 2010; 153: 403-419. https://doi.org/10.1104/pp.110.156000

Krumb M, Jager M, Voss A, Immig L, Peters K, Kowalczyk D, Bufe A, Opatz T, Holst O, Vogel C, Peters M. Total synthesis of a partial structure from arabinogalactan and its application for allergy-prevention. Chem-A Eur J 2020; 27(3): 928-933. https://doi.org/10.1002/chem.202002287

Leszczuk A, Kalaitzis P, Blazakis KN, Zdunek A. The role of arabinogalactan proteins in fruit ripening - A review. Hort Res 2020; 7: 176. https://doi.org/10.1038/s41438-020-00397-8

Rabinovich S, Silberman A, Adler L, Agron S, Levin-Zaidman S, Bahat A, Porat Z, Ben-Zeev E, Geva I, Itkin M, Malitsky S, Buchaklian A, Helbling D, Dimmock D, Erez A. The mitochondrial carrier Citrin plays a role in regulating cellular energy during carcinogenesis. Oncogene 2020; 39(1): 164-175. https://doi.org/10.1038/s41388-019-0976-2

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.