Remodelling of cell wall composition during leaf development in Lavoisiera mucorifera (Melastomataceae)
Kleber Resende Silva A , Vinícius Coelho Kuster B , Ana Flávia de Melo Silva A and Denis Coelho de Oliveira A C
+ Author Affiliations
- Author Affiliations
A Universidade Federal de Uberlândia, Instituto de Biologia; Laboratório de Anatomia, Desenvolvimento Vegetal e Interações; Campus Umuarama, CEP 38402-020, Uberlândia, Minas Gerais, Brazil.
B Universidade Federal de Goiás (UFG), Regional Jataí, Instituto de Biociências, Campus Cidade Universitária, BR 364, km 195, no. 3800, CEP 75801-615, Jataí, Goiás, Brazil.
C Corresponding author. Email: denisoliveira@ufu.br
Australian Journal of Botany 67(2) 140-148 https://doi.org/10.1071/BT18123
Submitted: 15 June 2018 Accepted: 18 March 2019 Published: 26 April 2019
Abstract
How does the deposition of cell wall components structure cell shape and function during leaf ontogenesis? Although this issue has been the subject of several studies, a wide variety of standards have been reported and many knowledge gaps remain. In this study we evaluated cell wall composition in leaf tissues of Lavoisiera mucorifera Mart. & Schrank ex DC. (Melastomataceae) regarding cellulose, pectin (homogalacturonans (HGs) and rhamnogalacturonans I (RGI)) and arabinogalactan protein (AGP) distribution during ontogenesis. Leaf primordium, as well as young and mature leaves, were submitted to histochemical analysis using calcofluor white and ruthenium red, and immunocytochemical analysis using primary monoclonal antibodies (JIM5, JIM7, LM2, LM5 and LM6). Results showed that the distribution of cell wall components depends on tissue and leaf developmental stage. At the beginning of cell differentiation in the leaf primordium, two main patterns of cellulose microfibril orientation occur: perpendicular and random. This initial microfibril arrangement determines final cell shape and leaf tissue functionality in mature leaves. During leaf development, especially in epidermal and collenchyma cells, the association of HGs with low methyl-esterified groups and cellulose guarantees mechanical support. As a result, cell wall properties, such as rigidity and porosity, may also be acquired by changes in cell wall composition and are associated with morphogenetic patterns in L. mucorifera.
Additional keywords: cellulose, homogalacturonans, monoclonal antibodies, ontogenesis, rhamnogalacturonans.
References
Albersheim P, Darvill A, Roberts K, Sederoff A, Staehelin A (2011) ‘Plant cell walls.’ (Garland Science, Taylor & Francis Group: New York)Baron-Epel O, Paramjit KG, Schindler M (1988) Pectins as mediators of wall porosity in soybean cells. Planta 175, 389–395.
| Pectins as mediators of wall porosity in soybean cells.Crossref | GoogleScholarGoogle Scholar | 24221876PubMed |
Baskin TI (2005) Anisotropic expansion of the plant cell wall. Annual Review of Cell and Developmental Biology 21, 203–222.
| Anisotropic expansion of the plant cell wall.Crossref | GoogleScholarGoogle Scholar | 16212493PubMed |
Ben Amar A, Cobanov P, Ghorbel A, Mliki A, Reustle GM (2010) Involvement of arabinogalactan proteins in the control of cell proliferation of Curcubita pepo suspension cultures. Biologia Plantarum 54, 321–324.
| Involvement of arabinogalactan proteins in the control of cell proliferation of Curcubita pepo suspension cultures.Crossref | GoogleScholarGoogle Scholar |
Brown RM (2004) Cellulose structure and biosynthesis: what is in store for the 21st century? Journal of Polymer Science. Part A, Polymer Chemistry 42, 487–495.
| Cellulose structure and biosynthesis: what is in store for the 21st century?Crossref | GoogleScholarGoogle Scholar |
Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydrate Research 344, 1879–1900.
| The structure, function, and biosynthesis of plant cell wall pectic polysaccharides.Crossref | GoogleScholarGoogle Scholar | 19616198PubMed |
Chebli Y, Geitmann A (2017) Cellular growth in plants requires regulation of cell wall biochemistry. Current Opinion in Cell Biology 44, 28–35.
| Cellular growth in plants requires regulation of cell wall biochemistry.Crossref | GoogleScholarGoogle Scholar | 28131101PubMed |
Clausen MH, Willats WGT, Knox JP (2003) Synthetic methyl hexagalacturonatehapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydrate Research 338, 1797–1800.
| Synthetic methyl hexagalacturonatehapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7.Crossref | GoogleScholarGoogle Scholar | 12892947PubMed |
Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annual Review of Cell and Developmental Biology 13, 171–201.
| Assembly and enlargement of the primary cell wall in plants.Crossref | GoogleScholarGoogle Scholar | 9442872PubMed |
Coutinho LM (2006) O conceito de bioma. Acta Botanica Brasilica 20, 13–23.
| O conceito de bioma.Crossref | GoogleScholarGoogle Scholar |
De Smet I, Beeckman T (2011) Asymmetric cell division in lend plants and algae: the driving force for differentiation. Nature Reviews. Molecular Cell Biology 12, 177–188.
| Asymmetric cell division in lend plants and algae: the driving force for differentiation.Crossref | GoogleScholarGoogle Scholar | 21346731PubMed |
Evert RF (2006) ‘Esau’s plant anatomy. Meristems, cells and tissues of the plant body – their structure function and development.’ (Wiley-Interscience: New Jersey)
Gao M, Showalter AM (1999) Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement. The Plant Journal 19, 321–331.
| Yariv reagent treatment induces programmed cell death in Arabidopsis cell cultures and implicates arabinogalactan protein involvement.Crossref | GoogleScholarGoogle Scholar | 10476079PubMed |
Guillon F, Moïse A, Quemener B, Bouchet B, Devaux MF, Alvarado C, Lahaye M (2017) Remodeling of pectin and hemicelluloses in tomato pericarp during fruit growth. Plant Science 257, 48–62.
| Remodeling of pectin and hemicelluloses in tomato pericarp during fruit growth.Crossref | GoogleScholarGoogle Scholar | 28224918PubMed |
Herth W, Sghnepf E (1980) The fluorochrome, calcofluor white, binds oriented to structural polysaccharide fibrils. Protoplasma 105, 129–133.
| The fluorochrome, calcofluor white, binds oriented to structural polysaccharide fibrils.Crossref | GoogleScholarGoogle Scholar |
Hijazi M, Roujol D, Nguyen-Kim H, Rocio Cisneros Castillo L, Saland E, Jamet E, Albenne C (2014) Arabinogalactan protein 31 (AGP31), a putative network-forming protein in Arabidopsis thaliana cell walls? Annals of Botany 114, 1087–1097.
| Arabinogalactan protein 31 (AGP31), a putative network-forming protein in Arabidopsis thaliana cell walls?Crossref | GoogleScholarGoogle Scholar | 24685714PubMed |
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytologist 189, 17–39.
| Epidermis: the formation and functions of a fundamental plant tissue.Crossref | GoogleScholarGoogle Scholar | 21054411PubMed |
Jensen WA (1962) ‘Botanical histochemistry.’ (W.H. Freeman & Co.: San Francisco, CA, USA)
Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-β-d-galactan. Plant Physiology 113, 1405–1412.
| Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1→4)-β-d-galactan.Crossref | GoogleScholarGoogle Scholar | 12223681PubMed |
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of Cell Biology 27, 137–138.
Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins; using salt stress to analyse AGP function. New Phytologist 169, 479–492.
| Salt stress upregulates periplasmic arabinogalactan proteins; using salt stress to analyse AGP function.Crossref | GoogleScholarGoogle Scholar |
Leroux O (2012) Collenchyma: a versatile mechanical tissue with dynamic cell walls. Annals of Botany 110, 1083–1098.
| Collenchyma: a versatile mechanical tissue with dynamic cell walls.Crossref | GoogleScholarGoogle Scholar | 22933416PubMed |
Leszczuk A, Szczuka E, Wydrych J, Zdunek A (2018) Changes in arabinogalactan proteins (AGPs) distribution in apple (Malus × domestica) fruit during senescence. Postharvest Biology and Technology 138, 99–106.
| Changes in arabinogalactan proteins (AGPs) distribution in apple (Malus × domestica) fruit during senescence.Crossref | GoogleScholarGoogle Scholar |
Levesque-Tremblay G, Pelloux J, Braybrook SA, Müller K (2015) Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta 242, 791–811.
| Tuning of pectin methylesterification: consequences for cell wall biomechanics and development.Crossref | GoogleScholarGoogle Scholar | 26168980PubMed |
Majewska-Sawka A, Nothnagel EA (2000) The multiple roles of arabinogalactan proteins in plant development. Plant Physiology 122, 3–9.
| The multiple roles of arabinogalactan proteins in plant development.Crossref | GoogleScholarGoogle Scholar | 10631243PubMed |
Mohnen D (2008) Pectin structure and biosynthesis. Current Opinion in Plant Biology 11, 266–277.
| Pectin structure and biosynthesis.Crossref | GoogleScholarGoogle Scholar | 18486536PubMed |
Obroucheva NV (2008) Cell elongation as an inseparable component of growth interrestrial plants. Russian Journal of Developmental Biology 39, 13–24.
| Cell elongation as an inseparable component of growth interrestrial plants.Crossref | GoogleScholarGoogle Scholar |
Oliveira DC, Magalhães TA, Ferreira BG, Teixeira CT, Formiga AT, Fernandes GW, Isaias RMS (2014) Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall. PLoS One 9, e94588
| Variation in the degree of pectin methylesterification during the development of Baccharis dracunculifolia kidney-shaped gall.Crossref | GoogleScholarGoogle Scholar | 25188326PubMed |
Peaucelle A, Louvet R, Johansen JN, Hofte H, Laufs P, Pelloux J, Mouille G (2008) Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Current Biology 18, 1943–1948.
| Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins.Crossref | GoogleScholarGoogle Scholar | 19097903PubMed |
Ridley B, O’Neil MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phtochemistry 57, 929–967.
| Pectins: structure, biosynthesis, and oligogalacturonide-related signaling.Crossref | GoogleScholarGoogle Scholar |
Rodriguez RE, Debernardi JM, Palatinik JF (2014) Morphogenesis of simple leaves: regulation of leaf size and shape. WIREs Developmental Biology 3, 41–57.
| Morphogenesis of simple leaves: regulation of leaf size and shape.Crossref | GoogleScholarGoogle Scholar | 24902833PubMed |
Sala K, Potocka I, Kurczynska E (2013) Spatio-temporal distribution and methyl-esterification of pectic epitopes provide evidence of developmental regulation of pectins during somatic embryogenesis in Arabidopsis thaliana. Biologia Plantarum 57, 410–416.
| Spatio-temporal distribution and methyl-esterification of pectic epitopes provide evidence of developmental regulation of pectins during somatic embryogenesis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annual Review of Plant Biology 58, 137–161.
| The biology of arabinogalactan proteins.Crossref | GoogleScholarGoogle Scholar | 17201686PubMed |
Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cellular and Molecular Life Sciences 58, 1399–1417.
| Arabinogalactan-proteins: structure, expression and function.Crossref | GoogleScholarGoogle Scholar | 11693522PubMed |
Silva KR, Oliveira DC (2014) Ontogênese foliar em Lavoisiera mucorifera Mart. & Schrank ex DC. (Melastomataceae). Bioscience Journal 30, 1241–1251.
Smallwood M, Yates EA, Willats WGT, Martin H, Knox JP (1996) Immunochemical comparison of membrane associated and secreted arabinogalactan-proteins in rice and carrot. Planta 198, 452–459.
| Immunochemical comparison of membrane associated and secreted arabinogalactan-proteins in rice and carrot.Crossref | GoogleScholarGoogle Scholar |
Somerville C (2006) Cellulose synthesis in higher plants. Annual Review of Cell and Developmental Biology 22, 53–78.
| Cellulose synthesis in higher plants.Crossref | GoogleScholarGoogle Scholar | 16824006PubMed |
Sterling C (1970) Crystal-structure of ruthenium red and stereochemistry of its pectic stain. American Journal of Botany 57, 172–175.
| Crystal-structure of ruthenium red and stereochemistry of its pectic stain.Crossref | GoogleScholarGoogle Scholar |
Sterling JD, Quigley HF, Orellana A, Mohnen D (2001) The catalytic site of pectin biosynthetic enzyme α-1,4-galacturonosyltransferase is located in the lumen of Golgi. Plant Physiology 127, 360–371.
| The catalytic site of pectin biosynthetic enzyme α-1,4-galacturonosyltransferase is located in the lumen of Golgi.Crossref | GoogleScholarGoogle Scholar | 11553763PubMed |
Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytologist 178, 239–252.
| Cellulose biosynthesis and deposition in higher plants.Crossref | GoogleScholarGoogle Scholar | 18298430PubMed |
Townsley BT, Sinha NR (2012) A new development: evolving concepts in leaf ontogeny. Annual Review of Plant Biology 63, 535–562.
| A new development: evolving concepts in leaf ontogeny.Crossref | GoogleScholarGoogle Scholar | 22404465PubMed |
Tsukaya H (2006) Mechanism of leaf-shape determination. Annual Review of Plant Biology 57, 477–496.
| Mechanism of leaf-shape determination.Crossref | GoogleScholarGoogle Scholar | 16669771PubMed |
Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009) An extended set of monoclonal antibodies to pectichomogalacturonan. Carbohydrate Research 344, 1858–1862.
| An extended set of monoclonal antibodies to pectichomogalacturonan.Crossref | GoogleScholarGoogle Scholar | 19144326PubMed |
Voragen AGJ, Coenen G-J, Verhoef RP, Schols HA (2009) Pectin, a versatile polysaccharide present in plant cell walls. Structural Chemistry 20, 263–275.
| Pectin, a versatile polysaccharide present in plant cell walls.Crossref | GoogleScholarGoogle Scholar |
Wang T, Park YB, Cosgrove DJ, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis primary cell walls: evidence from solid-state nuclear magnetic resonance. Plant Physiology 168, 871–884.
| Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis primary cell walls: evidence from solid-state nuclear magnetic resonance.Crossref | GoogleScholarGoogle Scholar | 26036615PubMed |
Willats WGT, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1→5)-α-L-arabinan. Carbohydrate Research 308, 149–152.
| Generation of a monoclonal antibody specific to (1→5)-α-L-arabinan.Crossref | GoogleScholarGoogle Scholar |
Willats WGT, Orfila C, Limberg G, Buchholt HC, Van Alebeek G-JWM, Voragen AGJ, Marcus SE, Christensen TMIE, Mikkelsen JD, Murray BS, Knox JP (2001) Modulation of the degree and pattern of methyl-esterification of pectichomogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. Journal of Biological Chemistry 276, 19404–19413.
| Modulation of the degree and pattern of methyl-esterification of pectichomogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion.Crossref | GoogleScholarGoogle Scholar |
Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249, S169–S175.
| Growth control by cell wall pectins.Crossref | GoogleScholarGoogle Scholar | 22215232PubMed |
Wolf S, Mouille G, Pelloux J (2009) Homogalacturonan methyl-esterification and plant development. Molecular Plant 2, 851–860.
| Homogalacturonan methyl-esterification and plant development.Crossref | GoogleScholarGoogle Scholar | 19825662PubMed |
Yates EA, Valdor JF, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6, 131–139.
| Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies.Crossref | GoogleScholarGoogle Scholar | 8727785PubMed |
