In vivo and ex vivo study on cell wall components as part of the network in tomato fruit during the ripening process

Nataliia Kutyrieva-Nowak , Agata Leszczuk , Dusan Denic , Samia Bellaidi , Konstantinos Blazakis , Petroula Gemeliari , Magdalena Lis , Panagiotis Kalaitzis , Artur Zdunek

Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) : 145

PDF (2568KB)
Horticulture Research ›› 2024, Vol. 11 ›› Issue (7) :145 DOI: 10.1093/hr/uhae145
Article
research-article
In vivo and ex vivo study on cell wall components as part of the network in tomato fruit during the ripening process
Author information +
History +
PDF (2568KB)

Abstract

Ripening is a process involving various morphological, physiological, and biochemical changes in fruits. This process is affected by modifications in the cell wall structure, particularly in the composition of polysaccharides and proteins. The cell wall assembly is a network of polysaccharides and proteoglycans named the arabinoxylan pectin arabinogalactan protein1 (APAP1). The complex consists of the arabinogalactan protein (AGP) core with the pectin domain including arabinogalactan (AG) type II, homogalacturonan (HG), and rhamnogalacturonan I (RG-I). The present paper aims to determine the impact of a disturbance in the synthesis of one constituent on the integrity of the cell wall. Therefore, in the current work, we have tested the impact of modified expression of the SlP4H3 gene connected with proline hydroxylase (P4H) activity on AGP presence in the fruit matrix. Using an immunolabelling technique (CLSM), an immunogold method (TEM), molecular tools, and calcium mapping (SEM-EDS), we have demonstrated that disturbances in AGP synthesis affect the entire cell wall structure. Changes in the spatio-temporal AGP distribution may be related to the formation of a network between AGPs with other cell wall components. Moreover, the modified structure of the cell wall assembly induces morphological changes visible at the cellular level during the progression of the ripening process. These results support the hypothesis that AGPs and pectins are required for the proper progression of the physiological processes occurring in fruits.

Cite this article

Download citation ▾
Nataliia Kutyrieva-Nowak, Agata Leszczuk, Dusan Denic, Samia Bellaidi, Konstantinos Blazakis, Petroula Gemeliari, Magdalena Lis, Panagiotis Kalaitzis, Artur Zdunek. In vivo and ex vivo study on cell wall components as part of the network in tomato fruit during the ripening process. Horticulture Research, 2024, 11 (7) : 145 DOI:10.1093/hr/uhae145

登录浏览全文

4963

注册一个新账户 忘记密码

Acknowledgements

This research was funded by the National Science Center, Poland (SONATA 16, grant number 2020/39/D/NZ9/00232). Also, this work has been supported by the COST Action ‘Roxy-COST’ (CA:18210) which is funded by the European Cooperation in Science & Technology. Also, work has been financed by the European Regional Development Fund of the European Union and Greek national funds through the Operational Competitiveness, Entrepreneurship and Innovation, under the call RESEARCH-CREATE-INNOVATE (project code: T2EDK-01332: n-Tomatomics - Development of new tomato cultivars by using -omics technologies).

Author contributions

N.K. Investigation, Methodology, Data curation, Visualization, Writing—original draft; A.L. Supervision, Project administration, Funding acquisition, Formal analysis, Writing—review & editing; M.L. Investigation (TEM imaging); D.D., S.B., K.B., P.G. Investigation (created the transgenic lines); P.K. Investigation (created the transgenic lines), Writing—review & editing; and A.Z. Writing—review & editing.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Data availability statement

The data underlying this article are available in the RepOD database [Leszczuk Agata, 2023, Studies on arabinogalactan proteins (AGPs) in fruits, file folder no A_6] at https://doi.org/10.18150/KMG7WI.

References

[1]

Wang D, Seymour GB. Molecular and biochemical basis of softening in tomato. Mol Hortic. 2022; 2 :1-10

[2]

Osorio S, Scossa F, Fernie AR. Molecular regulation of fruit ripening. Front Plant Sci. 2013; 4 :1-8

[3]

Mo Y, Jiang B, Huo J. et al. Quantitative ubiquitylomic analysis of the dynamic changes and extensive modulation of ubiquitylation in papaya during the fruit ripening process. Front Plant Sci. 2022; 13 :1-11

[4]

Castro RI, Morales-Quintana L. Study of the cell wall components produced during different ripening stages through thermogravimetric analysis. Cellulose. 2019; 26 :3009-20

[5]

Li S, Chen K, Grierson D. Molecular and hormonal mechanisms regulating fleshy fruit ripening. Cells. 2021; 10 :1-34

[6]

Huang B, Hu G, Wang K. et al. Interaction of two MADS-box genes leads to growth phenotype divergence of all-flesh type of tomatoes. Nat Commun. 2021; 12 :1-14

[7]

Kalaitzis P, Giannoutsou E, Konkina A. Role of the cell wall in the regulation of fruit ripening. In: Plant Cell Walls: Research Milestones and Conceptual Insights. Boca Raton: CRC Press, 2023,147-61

[8]

Jiang F, Lopez A, Jeon S. et al. Disassembly of the fruit cell wall by the ripening-associated polygalacturonase and expansin influences tomato cracking. Hortic Res. 2019; 6 :1-15

[9]

Li X, Wang X, Zhang Y. et al. Regulation of fleshy fruit ripening: from transcription factors to epigenetic modifications. Hortic Res. 2022; 9 :1-12

[10]

Guo Y, Bao Z, Deng Y. et al. Protein subcellular localization and functional studies in horticultural research: problems, solutions, and new approaches. Hortic Res. 2023; 10 :1-5

[11]

Tucker MR, Lou H, Aubert MK. et al. Exploring the role of cell wall-related genes and polysaccharides during plant development. Plan Theory. 2018; 7 :1-17

[12]

Hijazi M, Velasquez SM, Jamet E. et al. An update on post-translational modifications of hydroxyproline-rich glycoproteins: toward a model highlighting their contribution to plant cell wall architecture. Front Plant Sci. 2014; 5 :1-10

[13]

Srivastava V, McKee LS, Bulone V. Plant cell walls. In: eLS. Chichester; John Wiley & Sons, Ltd, 2017,1-17

[14]

Tucker G, Yin X, Zhang A. et al. Ethylene and fruit softening. Food Qual Saf. 2017; 1 :253-67

[15]

Posé S, Paniagua C, Matas AJ. et al. A nanostructural view of the cell wall disassembly process during fruit ripening and postharvest storage by atomic force microscopy. Trends Food Sci Technol. 2019; 87 :47-58

[16]

Scheller HV, Ulvskov P. Hemicelluloses. Annu Rev Plant Biol. 2010; 61 :263-89

[17]

Goulao LF, Oliveira CM. Cell wall modifications during fruit ripening: when a fruit is not the fruit. Trends Food Sci Technol. 2008; 19 :4-25

[18]

Zhang B, Gao Y, Zhang L. et al. The plant cell wall: biosynthesis, construction, and functions. J Integr Plant Biol. 2021; 63 :251-72

[19]

Curry TM, Peña MJ, Urbanowicz BR. An update on xylan structure, biosynthesis, and potential commercial applications. Cell Surf. 2023; 9 :1-4

[20]

Pauly M, Albersheim P, Darvill A. et al. Molecular domains of the cellulose/xyloglucan network in the cell walls of higher plants. Plant J. 1999; 20 :629-39

[21]

del Carmen Rodriguez-Gacio M, Iglesias-Fernandez R, Carbonero P. et al. Softening-up mannan-rich cell walls. J Exp Bot. 2012; 63 :3976-88

[22]

Paniagua C, Posé S, Morris VJ. et al. Fruit softening and pectin disassembly: an overview of nanostructural pectin modifications assessed by atomic force microscopy. Ann Bot. 2014; 114 :1375-83

[23]

Caffall KH, Mohnen D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res. 2009; 344 :1879-900

[24]

Engle KA, Amos RA, Yang JY. et al. Multiple Arabidopsis galacturonosyltransferases synthesize polymeric homogalacturonan by oligosaccharide acceptor-dependent or de novo synthesis. Plant J. 2022; 109 :1441-56

[25]

Ning T, Chen C, Yi G. et al. Changes in homogalacturonan metabolism in banana peel during fruit development and ripening. Int J Mol Sci. 2022; 23 :1-20

[26]

Yapo BM. Rhamnogalacturonan-I: a structurally puzzling and functionally versatile polysaccharide from plant cell walls and mucilages. Polymer Rev. 2011; 51 :391-413

[27]

Barnes WJ, Koj S, Black IM. et al. Protocols for isolating and characterizing polysaccharides from plant cell walls: a case study using rhamnogalacturonan-II. Biotechnol Biofuels. 2021; 14 :1-20

[28]

Brummell DA, Dal Cin V, Crisosto CH. et al. Cell wall metabolism during maturation, ripening and senescence of peach fruit. J Exp Bot. 2004; 55 :2029-39

[29]

Hyodo H, Terao A, Furukawa J. et al. Tissue specific localization of pectin-Ca 2 + cross-linkages and pectin methyl-esterification during fruit ripening in tomato ( Solanum lycopersicum ). PLoS One. 2013; 8 :1-10

[30]

Brummell DA. Sensing when the wall comes tumbling down. J Exp Bot. 2020; 71 :6865-8

[31]

Orfila C, Seymour GB, Willats WG. et al. Altered middle lamella homogalacturonan and disrupted deposition of (1-5)-L-arabinan in the pericarp of Cnr, a ripening mutant of tomato. Plant Physiol. 2001; 126 :210-21

[32]

Orfila C, Huisman MMH, Willats WGT. et al. Altered cell wall disassembly during ripening of Cnr tomato fruit: implications for cell adhesion and fruit softening. Planta. 2002; 215 :440-7

[33]

Brummell DA, Harpster MH. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol. 2001; 47 :311-39

[34]

Harholt J, Suttangkakul A, Scheller HV. Biosynthesis of pectin. Plant Physiol. 2010; 153 :384-95

[35]

Silva J, Ferraz R, Dupree P. et al. Three decades of advances in arabinogalactan-protein biosynthesis. Front Plant Sci. 2020; 11 :1-18

[36]

Cooper JB, Heuser JE, Varner JE. 3,4-Dehydroproline inhibits cell wall assembly and cell division in tobacco protoplasts. Plant Physiol. 1994; 104 :747-52

[37]

Jamet E, Canut H, Boudart G. et al. Cell wall proteins: a new insight through proteomics. Trends Plant Sci. 2006; 11 :33-9

[38]

Parra R, Gomez-Jimenez MC. Spatio-temporal immunolocalization of extensin protein and hemicellulose polysaccharides during olive fruit abscission. Planta. 2020; 252 :1-15

[39]

Kieliszewski MJ, Lamport DTA. Entensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J. 1994; 5 :157-72

[40]

Leszczuk A, Kalaitzis P, Kulik J. et al. Review: structure and modifications of arabinogalactan proteins (AGPs). BMC Plant Biol. 2023; 23 :1-12

[41]

Hromadova D, Soukup A, Tylova E. Arabinogalactan proteins in plant roots - an update in possible functions. Front Plant Sci. 2021; 12 :1-15

[42]

Tsumuraya Y, Ozeki E, Ooki Y. et al. Properties of arabinogalactan-proteins in European pear ( Pyrus communis L.) fruits. Carbohydr Res. 2019; 485 :1-9

[43]

Kutyrieva-Nowak N, Leszczuk A, Zając A. et al. Arabinogalactan protein is a molecular and cytological marker of particular stages of the tomato fruit ripening process. Sci Hortic. 2023; 310 :111718-0

[44]

Leszczuk A, Kalaitzis P, Blazakis KN. et al. The role of arabinogalactan proteins (AGPs) in fruit ripening - a review. Hort Res. 2020; 7 :1-12

[45]

Tan L, Eberhard S, Pattathil S. et al. An Arabidopsis cell wall proteoglycan consists of pectin and arabinoxylan covalently linked to an arabinogalactan protein. Plant Cell. 2013; 25 :270-87

[46]

Fry SC. Isodityrosine, a new cross-linking amino acid from plant cell-wall glycoprotein. Biochem J. 1982; 204 :449-55

[47]

Ellis M, Egelund J, Schultz CJ. et al. Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol. 2010; 153 :403-19

[48]

Tan L, Zhang L, Black I. et al. Most of the rhamnogalacturonan-I from cultured Arabidopsis cell walls is covalently linked to arabinogalactan-protein. Carbohydr Polym. 2023; 301 :120340-12

[49]

Brummell DA. Cell wall disassembly in ripening fruit. Funct Plant Biol. 2006; 33 :103-19

[50]

Zhang W, Guo M, Yang W. et al. The role of cell wall polysaccharides disassembly and enzyme activity changes in the softening process of Hami melon ( Cucumis melo L.). Food Secur. 2022; 11 :1-20

[51]

Forlani S, Masiero S, Mizzotti C. Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens. J Exp Bot. 2019; 70 :2993-3006

[52]

Redgwell RJ, MacRae E, Hallett I. et al. In vivo and in vitro swelling of cell walls during fruit ripening. Planta. 1997; 203 :162-73

[53]

Lopez-Hernandez F, Tryfona T, Rizza A. et al. Calcium binding by arabinogalactan polysaccharides is important for normal plant development. Plant Cell. 2020; 32 :3346-69

[54]

Pfeifer L, Shafee T, Johnson KL. et al. Arabinogalactan-proteins of Zostera marina L. contain unique glycan structures and provide insight into adaption processes to saline environments. Sci Rep. 2020; 10 :1-10

[55]

Tan L, Qiu F, Lamport DTA. et al. Structure of a hydroxyproline (Hyp)-arabinogalactan polysaccharide from repetitive ala-Hyp expressed in transgenic Nicotiana tabacum. J Biol Chem. 2004; 279 :13156-65

[56]

Willats WGT, Orfila C, Limberg G. et al. Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls: implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem. 2001; 276 :19404-13

[57]

Lamport DTA, Várnai P. Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol. 2013; 197 :58-64

[58]

Lamport DTA, Tan L, Held M. et al. Pollen tube growth and guidance: Occam’s razor sharpened on a molecular arabinogalactan glycoprotein Rosetta Stone. New Phytol. 2018; 217 :491-500

[59]

Knoch E, Dilokpimol A, Tryfona T. et al. A β-glucuronosyltransferase from Arabidopsis thaliana involved in biosynthesis of type II arabinogalactan has a role in cell elongation during seedling growth. Plant J. 2013; 76 :1016-29

[60]

Ajayi OO, Held MA, Showalter AM. Three β-glucuronosyltransferase genes involved in arabinogalactan biosynthesis function in Arabidopsis growth and development. Plan Theory. 2021; 10 :1-19

[61]

Zhang Y, Held MA, Showalter AM. Elucidating the roles of three β-glucuronosyltransferases (GLCATs) acting on arabinogalactan-proteins using a CRISPR-Cas 9 multiplexing approach in Arabidopsis. BMC Plant Biol. 2020; 20 :1-20

[62]

Demarty M, Morvan C. Calcium and the cell wall. Plant Cell Environ. 1984; 7 :441-8

[63]

Michailidis M, Karagiannis E, Tanou G. et al. Novel insights into the calcium action in cherry fruit development revealed by high-throughput mapping. Plant Mol Biol. 2020; 104 :597-614

[64]

Hocking B, Tyerman SD, Burton RA. et al. Fruit calcium: transport and physiology. Front Plant Sci. 2016; 7 :1-17

[65]

Xiong T, Tan Q, Li S. et al. Interactions between calcium and ABA signaling pathways in the regulation of fruit ripening. J Plant Physiol. 2021; 256 :153309-30

[66]

Xu W, Peng H, Yang T. et al. Effect of calcium on strawberry fruit flavonoid pathway gene expression and anthocyanin accumulation. Plant Physiol Biochem. 2014; 82 :289-98

[67]

Kutyrieva-Nowak N, Leszczuk A, Ezzat L. et al. The modified activity of prolyl 4 hydroxylases reveals the effect of arabinogalactan proteins on changes in the cell wall during the tomato ripening process. Front Plant Sci. 2024; 15 :1-21

[68]

Perrakis A, Denic D, Blazakis KN. et al. A tomato prolyl-4-hydroxylase causes relocation of abscission zone and alters abscission kinetics. bioRxiv. 2021; 04.20.440677 ;1-36

[69]

Perrakis A, Bita CE, Arhondakis S. et al. Suppression of a prolyl 4 hydroxylase results in delayed abscission of overripe tomato fruits. Front Plant Sci. 2019; 10 :1-11

[70]

Stafstrom JP, Staehelin LA. Antibody localization of extensin in cell walls of carrot storage roots. Planta. 1988; 174 :321-32

[71]

Barrelt DM, Gonzalez C. Activity of softening enzymes during cherry maturation. J Food Sci. 1994; 59 :574-7

[72]

Jarvis MC. Structure of native cellulose microfibrils, the starting point for nanocellulose manufacture. Philos Trans Royal Soc A. 2018; 376 :1-13

[73]

Rosli HG, Civello PM, Martínez GA. Changes in cell wall composition of three Fragaria × ananassa cultivars with different softening rate during ripening. Plant Physiol Biochem. 2004; 42 :823-31

[74]

Liu J, Ma Q, Liu D. et al. Identification of the cell wall proteins associated with the softening of Lycium barbarum L. fruit by using iTRAQ technology. Food Chem: Mol Sci. 2022; 4 :100-10

[75]

Posé S, Marcus SE, Knox JP. Differential metabolism of pectic galactan in tomato and strawberry fruit: detection of the LM26 branched galactan epitope in ripe strawberry fruit. Physiol Plant. 2018; 164 :95-105

[76]

Biswal AK, Atmodjo MA, Pattathil S. et al. Working towards recalcitrance mechanisms: increased xylan and homogalacturonan production by overexpression of GAlactUronosylTransferase 12 (GAUT12) causes increased recalcitrance and decreased growth in Populus Mike Himmel. Biotechnol Biofuels. 2018; 11 :1-26

[77]

Persson S, Caffall KH, Freshour G. et al. The Arabidopsis irregular xylem8 mutant is deficient in glucuronoxylan and homogalacturonan, which are essential for secondary cell wall integrity. Plant Cell. 2007; 19 :237-55

[78]

Peña MJ, Zhong R, Zhou GK. et al. Arabidopsis irregular xylem8 and irregular xylem9: implications for the complexity of glucuronoxylan biosynthesis. Plant Cell. 2007; 19 :549-63

[79]

Brown DM, Goubet F, Wong VW. et al. Comparison of five xylan synthesis mutants reveals new insight into the mechanisms of xylan synthesis. Plant J. 2007; 52 :1154-68

[80]

Fragkostefanakis S, Sedeek KEM, Raad M. et al. Virus induced gene silencing of three putative prolyl 4-hydroxylases enhances plant growth in tomato ( Solanum lycopersicum ). Plant Mol Biol. 2014; 85 :459-71

[81]

Nibbering P, Petersen BL, Motawia MS. et al. Golgi-localized exo-b1,3-galactosidases involved in cell expansion and root growth in Arabidopsis. J Biol Chem. 2020; 295 :10581-92

[82]

Tryfona T, Liang H-C, Kotake T. et al. Structural characterization of Arabidopsis leaf arabinogalactan polysaccharides. Plant Physiol. 2012; 160 :653-66

[83]

Hijazi M, Roujol D, Nguyen-Kim H. et al. Arabinogalactan protein 31 (AGP31), a putative network-forming protein in Arabidopsis thaliana cell walls? Ann Bot. 2014; 114 :1087-97

[84]

De Freitas ST, Handa AK, Wu Q. et al. Role of pectin methylesterases in cellular calcium distribution and blossom-end rot development in tomato fruit. Plant J. 2012; 71 :824-35

[85]

Chirinos X, Ying S, Rodrigues MA. et al. Transition to ripening in tomato requires hormone-controlled genetic reprogramming initiated in gel tissue. Plant Physiol. 2023; 191 :610-25

[86]

Liu Y, Shi Y, Su D. et al. SlGRAS4 accelerates fruit ripening by regulating ethylene biosynthesis genes and SlMADS1 in tomato. Hortic Res. 2021; 8 :1-11

[87]

Gan L, Song M, Wang X. et al. Cytokinins are involved in regulation of tomato pericarp thickness and fruit size. Hortic Res. 2022; 9 :1-10

[88]

Zou J, Li N, Hu N. et al. Co-silencing of ABA receptors (SlRCAR) reveals interactions between ABA and ethylene signaling during tomato fruit ripening. Hortic Res. 2022; 9 :1-15

[89]

Su D, Liu K, Yu Z. et al. Genome-wide characterization of the tomato GASA family identifies SlGASA 1 as a repressor of fruit ripening. Hortic Res. 2023; 10 :1-11

[90]

Wu M, Liu K, Li H. et al. Gibberellins involved in fruit ripening and softening by mediating multiple hormonal signals in tomato. Hortic Res. 2024; 11 :1-11

[91]

Konkina A, Klepadlo M, Lakehal A. et al. An Arabidopsis prolyl 4-hydroxylase is involved in the low oxygen response. Front Plant Sci. 2021; 12 :1-12

[92]

Gibbs DJ, Lee SC, Md Isa N. et al. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature. 2011; 479 :415-8

[93]

Weits DA, Giuntoli B, Kosmacz M. et al. Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat Commun. 2014; 5 :1-10

[94]

Batu A. Determination of acceptable firmness and colour values of tomatoes. J Food Eng. 2004; 61 :471-5

[95]

Nakatsuka A, Murachi S, Okunishi H. et al. Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase, and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol. 1998; 118 :1295-305

[96]

Kutyrieva-Nowak N, Leszczuk A, Zdunek A. A practical guide to in situ and ex situ characterisation of arabinogalactan proteins (AGPs) in fruits. Plant Methods. 2023; 19 :1-18

[97]

Moller I, Sørensen I, Bernal AJ. et al. High-throughput mapping of cell-wall polymers within and between plants using novel microarrays. Plant J. 2007; 50 :1118-28

[98]

Li W, Xu F, Chen S. et al. A comparative study on Ca content and distribution in two Gesneriaceae species reveals distinctive mechanisms to cope with high rhizospheric soluble calcium. Front Plant Sci. 2014; 5 :1-14

[99]

Qiu L, Wang Y, Qu H. Loading calcium fluorescent probes into protoplasts to detect calcium in the flesh tissue cells of Malus domestica. Hortic Res. 2020; 7 :1-11

PDF (2568KB)

114

Accesses

0

Citation

Detail

Sections
Recommended

/