Saltbush seedlings (Atriplex spp.) shed border-like cells from closed-type root apical meristems
Alison R. Gill
A and Rachel A. Burton A *
A
Abstract
Australian saltbush (Atriplex spp.) survive in exceptionally saline environments and are often used for pasture in semi-arid areas. To investigate the impact of salinity on saltbush root morphology and root exudates, three Australian native saltbush species (Atriplex nummularia, Atriplex amnicola, and Atriplex vesicaria) were grown in vitro in optimised sterile, semi-hydroponic systems in media supplemented with different concentrations of salt (NaCl). Histological stains and chromatographic techniques were used to characterise the root apical meristem (RAM) type and root exudate composition of the saltbush seedlings. We report that saltbush species have closed-type RAMs, which release border-like cells (BLCs). Monosaccharide content, including glucose and fructose, in the root mucilage of saltbush was found to be uniquely low, suggesting that saltbush may minimise carbon release in polysaccharides of root exudates. Root mucilage also contained notable levels of salt, plus increasing levels of unidentified compounds at peak salinity. Un-esterified homogalacturonan, xyloglucan, and arabinogalactan proteins between and on the surface of BLCs may aid intercellular adhesion. At the highest salinity levels, root cap morphology was altered but root:shoot ratio remained consistent. While questions remain about the identity of some components in saltbush root mucilage other than the key monosaccharides, this new information about root cap morphology and cell surface polysaccharides provides avenues for future research.
Keywords: Atriplex spp., border-like cells, homogalacturonan, monosaccharides, root apical meristem, root exudates, root morphology, root mucilage, salinity, Saltbush.
References
Amicucci MJ, Galermo AG, Guerrero A, et al. (2019) A strategy for structural elucidation of polysaccharides: elucidation of a maize mucilage that harbors diazotrophic bacteria. Analytical Chemistry 91(11), 7254-7265.
| Crossref | Google Scholar |
Aslam Z, Jeschke WD, Barrett-Lennard EG, et al. (1986) Effects of external NaCl on the growth of Atriplex amnicola and the ion relations and carbohydrate status of the leaves. Plant, Cell & Environment 9, 571-580.
| Crossref | Google Scholar |
Bacic A, Moody SF, Clarke AE (1986) Structural analysis of secreted root slime from maize (Zea mays L.). Plant Physiology 80, 771-777.
| Crossref | Google Scholar |
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant, Cell and Environment 32, 666-681.
| Crossref | Google Scholar |
Baetz U, Martinoia E (2014) Root exudates: the hidden part of plant defense. Trends in Plant Science 19, 90-98.
| Crossref | Google Scholar |
Bais HP, Weir TL, Perry LG, et al. (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 57, 233-266.
| Crossref | Google Scholar |
Baranova EN, Chaban IA, Kononenko NV, et al. (2019) Ultrastructural changes of organelles in root cap cells of tobacco under salinity. Proceedings of the Latvian Academy of Sciences, Section B: Natural, Exact, and Applied Sciences 73, 47-55.
| Crossref | Google Scholar |
Burton RA, Collins HM, Kibble NAJ, et al. (2011) Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1,3;1,4)-β-d-glucans and alters their fine structure. Plant Biotechnology Journal 9, 117-135.
| Crossref | Google Scholar |
Byrt CS, Munns R, Burton RA, et al. (2018) Root cell wall solutions for crop plants in saline soils. Plant Science 269, 47-55.
| Crossref | Google Scholar |
Chai YN, Schachtman DP (2022) Root exudates impact plant performance under abiotic stress. Trends in Plant Science 27, 80-91.
| Crossref | Google Scholar |
del Campillo E, Abdel-Aziz A, Crawford D, Patterson SE (2004) Root cap specific expression of an endo-β-1,4-d-glucanase (cellulase): a new marker to study root development in Arabidopsis. Plant Molecular Biology 56, 309-323.
| Crossref | Google Scholar |
Descheemaeker K, Smith AP, Robertson MJ, et al. (2014) Simulation of water-limited growth of the forage shrub saltbush (Atriplex nummularia Lindl.) in a low-rainfall environment of southern Australia. Crop & Pasture Science 65, 1068-1083.
| Crossref | Google Scholar |
Driouich A, Durand C, Vicré-Gibouin M (2007) Formation and separation of root border cells. Trends in Plant Science 12, 14-19.
| Crossref | Google Scholar |
Driouich A, Durand C, Cannesan MA, et al. (2010) Border cells versus border-like cells: are they alike? Journal of Experimental Botany 61, 3827-3831.
| Crossref | Google Scholar |
Driouich A, Gaudry A, Pawlak B, Moore JP (2021) Root cap-derived cells and mucilage: a protective network at the root tip. Protoplasma 258, 1179-1185.
| Crossref | Google Scholar |
Durand C, Vicre-Gibouin M, Follet-Gueye ML, et al. (2009) The organization pattern of root border-like cells of Arabidopsis is dependent on cell wall homogalacturonan. Plant Physiology 150, 1411-1421.
| Crossref | Google Scholar |
Ghanem ME, Han RM, Classen B, et al. (2010) Mucilage and polysaccharides in the halophyte plant species Kosteletzkya virginica: localization and composition in relation to salt stress. Journal of Plant Physiology 167, 382-392.
| Crossref | Google Scholar |
Groot EP, Doyle JA, Nichol SA, Rost TL (2004) Phylogenetic distribution and evolution of root apical meristem organization in dicotyledonous angiosperms. International Journal of Plant Sciences 165, 97-105.
| Crossref | Google Scholar |
Hamamoto L, Hawes MC, Rost TL (2006) The production and release of living root cap border cells is a function of root apical meristem type in dicotyledonous angiosperm plants. Annals of Botany 97, 917-923.
| Crossref | Google Scholar |
Harrington BJ, Hageage GJ (2003) Calcofluor White: a review of its uses and applications in clinical mycology and parasitology. Laboratory Medicine 34, 361-367.
| Crossref | Google Scholar |
Hawes M, Allen C, Turgeon BG, et al. (2016) Root border cells and their role in plant defense. Annual Review of Phytopathology 54, 143-161.
| Crossref | Google Scholar |
Hayashi T, Kaida R (2011) Functions of xyloglucan in plant cells. Molecular Plant 4, 17-24.
| Crossref | Google Scholar |
Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Critical Reviews in Plant Sciences 30, 435-458.
| Crossref | Google Scholar |
Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant and Soil 321, 5-33.
| Crossref | Google Scholar |
Kawasaki A, Donn S, Ryan PR, et al. (2016) Microbiome and exudates of the root and rhizosphere of Brachypodium distachyon, a model for wheat. PLoS ONE 11, 1-25.
| Crossref | Google Scholar |
Kawasaki A, Okada S, Zhang C, et al. (2018) A sterile hydroponic system for characterising root exudates from specific root types and whole - root systems of large crop plants. Plant Methods 14, 114.
| Crossref | Google Scholar |
Kiani-Pouya A, Roessner U, Jayasinghe NS, et al. (2017) Epidermal bladder cells confer salinity stress tolerance in the halophyte quinoa and Atriplex species. Plant, Cell & Environment 40, 1900-1915.
| Crossref | Google Scholar |
Knee EM, Gong F-C, Gao M, et al. (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Molecular Plant-Microbe Interactions 14, 775-784.
| Crossref | Google Scholar |
Knox OGG, Curlango-Rivera G, Huskey DA, Hawes MC (2020) Border cell counts of Bollgard3 cotton and extracellular DNA expression levels. Euphytica 216, 142.
| Crossref | Google Scholar |
Kumar N, Iyer-Pascuzzi AS (2020) Shedding the last layer: mechanisms of root cap cell release. Plants 9, 308.
| Crossref | Google Scholar |
Kumpf RP, Nowack MK (2015) The root cap: a short story of life and death. Journal of Experimental Botany 66, 5651-5662.
| Crossref | Google Scholar |
Lutts S, Qin P, Han RM (2016) Salinity influences biosorption of heavy metals by the roots of the halophyte plant species Kosteletzkya pentacarpos. Ecological Engineering 95, 682-689.
| Crossref | Google Scholar |
McCully ME (1999) Roots in soil: unearthing the complexities of roots and their rhizospheres. Annual Review of Plant Physiology and Plant Molecular Biology 50, 695-718.
| Crossref | Google Scholar |
Moody SF, Clarke AE, Bacic A (1988) Structural analysis of secreted slime from wheat and cowpea roots. Phytochemistry 27, 2857-2861.
| Crossref | Google Scholar |
Mravec J (2017) Border cell release: cell separation without cell wall degradation? Plant Signaling & Behavior 12, e1343778.
| Crossref | Google Scholar |
Nazari M (2021) Plant mucilage components and their functions in the rhizosphere. Rhizosphere 18, 100344.
| Crossref | Google Scholar |
Nedjimi B (2014) Effects of salinity on growth, membrane permeability and root hydraulic conductivity in three saltbush species. Biochemical Systematics and Ecology 52, 4-13.
| Crossref | Google Scholar |
Ninmanont P, Wongchai C, Pfeiffer W, Chaidee A (2021) Salt stress of two rice varieties: root border cell response and multi-logistic quantification. Protoplasma 258, 1119-1131.
| Crossref | Google Scholar |
Norman H, Wilmot M, Hulm E, Young P (2017) Developing perennial shrubs to fill feed gaps on marginal soils in Australia. In: ‘Grassland resources for extensive farming systems in marginal lands: major drivers and future scenarios. Proceedings of the 19th Symposium of the European Grassland Federation’. (Eds C Porqueddu, A Franca, G Lombardi, et al.) pp. 79–81. (European Grassland Federation)
Oburger E, Jones DL (2018) Sampling root exudates – mission impossible? Rhizosphere 6, 116-133.
| Crossref | Google Scholar |
Pelloux J, Rusterucci C, Mellerowicz E (2007) New insights into pectin methylesterase structure and function. Trends in Plant Science 12, 267-277.
| Crossref | Google Scholar |
Phan JL, Tucker MR, Khor SF, et al. (2016) Differences in glycosyltransferase family 61 accompany variation in seed coat mucilage composition in Plantago spp. Journal of Experimental Botany 67, 6481-6495.
| Crossref | Google Scholar |
Proseus TE, Boyer JS (2012) Pectate chemistry links cell expansion to wall deposition in Chara corallina. Plant Signaling & Behavior 7, 1490-1492.
| Crossref | Google Scholar |
Ray TC, Callow JA, Kennedy JF (1988) Composition of root mucilage polysaccharides from Lepidium sativum. Journal of Experimental Botany 39, 1249-1261.
| Crossref | Google Scholar |
Ropitaux M, Bernard S, Follet-Gueye M-L, et al. (2019) Xyloglucan and cellulose form molecular cross-bridges connecting root border cells in pea (Pisum sativum). Plant Physiology and Biochemistry 139, 191-196.
| Crossref | Google Scholar |
Rost TL (2011) The organization of roots of dicotyledonous plants and the positions of control points. Annals of Botany 107, 1213-1222.
| Crossref | Google Scholar |
Saito S, Niki T, Gladish DK (2019) Comparison of promeristem structure and ontogeny of procambium in primary roots of Zea mays ssp. Mexicana and Z. mays “Honey Bantam” with emphasis on metaxylem vessel histogenesis. Plants 8, 162.
| Crossref | Google Scholar |
Sasse J, Martinoia E, Northen T (2018) Feed your friends: do plant exudates shape the root microbiome? Trends in Plant Science 23, 25-41.
| Crossref | Google Scholar |
Stephenson MB, Hawes MC (1994) Correlation of pectin methylesterase activity in root caps of pea with root border cell separation. Plant Physiology 106, 739-745.
| Crossref | Google Scholar |
Tenhaken R (2015) Cell wall remodeling under abiotic stress. Frontiers in Plant Science 5, 771.
| Crossref | Google Scholar |
Ursache R, Andersen TG, Marhavý P, Geldner N (2018) A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. Plant Journal 93, 399-412.
| Crossref | Google Scholar |
Verhertbruggen Y, Marcus SE, Haeger A, et al. (2009) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydrate Research 344, 1858-1862.
| Crossref | Google Scholar |
Willats WGT, Orfila C, Limberg G, et al. (2001) Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Journal of Biological Chemistry 276, 19404-19413.
| Crossref | Google Scholar |
Wolf S, Mravec J, Greiner S, et al. (2012) Plant cell wall homeostasis is mediated by brassinosteroid feedback signaling. Current Biology 22, 1732-1737.
| Crossref | Google Scholar |
Zickenrott I-M, Woche SK, Bachmann J, et al. (2016) An efficient method for the collection of root mucilage from different plant species—a case study on the effect of mucilage on soil water repellency. Journal of Plant Nutrition and Soil Science 179, 294-302.
| Crossref | Google Scholar |
