Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Tripogon loliiformis elicits a rapid physiological and structural response to dehydration for desiccation tolerance

Mohammad Reza Karbaschi A , Brett Williams A , Acram Taji B and Sagadevan G. Mundree A C
+ Author Affiliations
- Author Affiliations

A Centre for Tropical Crops and Biocommodities, Queensland University of Technology, PO Box 2434, Brisbane, Qld 4001, Australia.

B School of Earth, Environmental and Biological Sciences, Science and Engineering Faculty, Queensland University of Technology, M Block Level 5, 528, Brisbane, Qld, 4001, Australia.

C Corresponding author. Email: sagadevan.mundree@qut.edu.au

Functional Plant Biology 43(7) 643-655 https://doi.org/10.1071/FP15213
Submitted: 28 July 2015  Accepted: 7 November 2015   Published: 5 February 2016

Abstract

Resurrection plants can withstand extreme dehydration to an air-dry state and then recover upon receiving water. Tripogon loliiformis (F.Muell.) C.E.Hubb. is a largely uncharacterised native Australian desiccation-tolerant grass that resurrects from the desiccated state within 72 h. Using a combination of structural and physiological techniques the structural and physiological features that enable T. loliiformis to tolerate desiccation were investigated. These features include: (i) a myriad of structural changes such as leaf folding, cell wall folding and vacuole fragmentation that mitigate desiccation stress, (ii) potential role of sclerenchymatous tissue within leaf folding and radiation protection, (iii) retention of ~70% chlorophyll in the desiccated state, (iv) early response of photosynthesis to dehydration by 50% reduction and ceasing completely at 80 and 70% relative water content, respectively, (v) a sharp increase in electrolyte leakage during dehydration, and (vi) confirmation of membrane integrity throughout desiccation and rehydration. Taken together, these results demonstrate that T. loliiformis implements a range of structural and physiological mechanisms that minimise mechanical, oxidative and irradiation stress. These results provide powerful insights into tolerance mechanisms for potential utilisation in the enhancement of stress-tolerance in crop plants.

Additional keywords: electrolyte leakage, leaf structure, membrane integrity, photosynthesis, physiology, resurrection plant.


References

Aldea M, Frank TD, DeLucia EH (2006) A method for quantitative analysis of spatially variable physiological processes across leaf surfaces. Photosynthesis Research 90, 161–172.
A method for quantitative analysis of spatially variable physiological processes across leaf surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsFyitA%3D%3D&md5=a90a59ac24083dfd86bc6a9d8552ecdcCAS | 17211583PubMed |

Alpert P, Oliver MJ (2002) Drying without dying. In ‘Desiccation and survival in plants’. (Eds M Black, HW Pritchard) pp. 4–31. (CABI: Wallingford, UK)

Alvarez JM, Rocha JF, Machado SR (2008) Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): structure in relation to function. Brazilian Archives of Biology and Technology 51, 113–119.
Bulliform cells in Loudetiopsis chrysothrix (Nees) Conert and Tristachya leiostachya Nees (Poaceae): structure in relation to function.Crossref | GoogleScholarGoogle Scholar |

Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=99fa8bbb1f5b69ffca6fc56116a2dc3fCAS | 15377225PubMed |

Bajji M, Kinet JM, Lutts S (2002) The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat. Plant Growth Regulation 36, 61–70.
The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Gmtbo%3D&md5=ef42d156d51ff4b057082de46e0c7ffdCAS |

Barthlott W, Neinhuis C, Cutler D, Ditsch F, Meusel I, Theisen I, Wilhelmi H (1998) Classification and terminology of plant epicuticular waxes. Botanical Journal of the Linnean Society 126, 237–260.
Classification and terminology of plant epicuticular waxes.Crossref | GoogleScholarGoogle Scholar |

Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43, 83–116.
Superoxide dismutase and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltVyjsb0%3D&md5=b53b978c73856711da52b0a310841df9CAS |

Brown RH (1999) Agronomic implications of C4 photosynthesis. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 473–507. (Academic Press: San Diego, CA, USA)

Clayton WD, Vorontsova MS, Harman KT, Williamson H (2010) ‘GrassBase - The Online World Grass Flora.’ Available at http://www.kew.org/data/grasses-db/www/imp10520.htm [Verified 30 November 2015]

Conley MM, Kimball B, Brooks T, Pinter P, Hunsaker D, Wall G, Adam N, LaMorte R, Matthias A, Thompson T (2001) CO2 enrichment increases water‐use efficiency in sorghum. New Phytologist 151, 407–412.
CO2 enrichment increases water‐use efficiency in sorghum.Crossref | GoogleScholarGoogle Scholar |

Corlett JE, Jones HG, Massacci A, Masojidek J (1994) Water deficit, leaf rolling and susceptibility to photoinhibition in field grown sorghum. Physiologia Plantarum 92, 423–430.
Water deficit, leaf rolling and susceptibility to photoinhibition in field grown sorghum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXitFersLc%3D&md5=f96afebd13bea47b919163cce6c3d092CAS |

Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annual Review of Plant Physiology 33, 317–345.
Stomatal conductance and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XktlKjs7o%3D&md5=f3189a8b2c17ebc7e2a997a6ff71f3e2CAS |

Farrant JM (2000) A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species. Plant Ecology 151, 29–39.
A comparison of mechanisms of desiccation tolerance among three angiosperm resurrection plant species.Crossref | GoogleScholarGoogle Scholar |

Farrant JM, Vander Willigen C, Loffell DA, Bartsch S, Whittaker A (2003) An investigation into the role of light during desiccation of three angiosperm resurrection plants. Plant, Cell & Environment 26, 1275–1286.
An investigation into the role of light during desiccation of three angiosperm resurrection plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsVCgtLw%3D&md5=10e94513a7ca4d86ebf36de92e63b21cCAS |

Farrant J, Cooper K, Hilgart A, Abdalla K, Bentley J, Thomson J, Dace HW, Peton N, Mundree S, Rafudeen M (2015) A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker). Planta 242, 407–426.
A molecular physiological review of vegetative desiccation tolerance in the resurrection plant Xerophyta viscosa (Baker).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXovVahtrs%3D&md5=4a81fdf3b34ee1b5b4a8347d18865fb1CAS | 25998524PubMed |

Flexas J, Medrano H (2002) Drought‐inhibition of photosynthesis in C3 plants: stomatal and non‐stomatal limitations revisited. Annals of Botany 89, 183–189.
Drought‐inhibition of photosynthesis in C3 plants: stomatal and non‐stomatal limitations revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkslymsLs%3D&md5=23430a053c49ba567760cc7a92fde2daCAS | 12099349PubMed |

Gaff DF (1971) Desiccation-tolerant flowering plants in southern Africa. Science 174, 1033–1034.
Desiccation-tolerant flowering plants in southern Africa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cvgtlOqtg%3D%3D&md5=1e1bf4edd6191257615db202968a25baCAS | 17757031PubMed |

Gaff DF (1981) ‘The biology of resurrection plants.’ In ‘The biology of Australian plants’. (Eds JS Pate, AJ Mc Comb) pp. 114–146. (University of Western Australia Press: Perth)

Gaff D, McGregor G (1979) The effect of dehydration and rehydration on the nitrogen content of various fractions from resurrection plants. Biologia Plantarum 21, 92–99.
The effect of dehydration and rehydration on the nitrogen content of various fractions from resurrection plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXitVSlsbs%3D&md5=06e35b6ec3c6f9c6ac9262ce7bf5f38eCAS |

Gaff DF, Blomstedt CK, Neale AD, Le TN, Hamill JD, Ghasempour HR (2009) Sporobolus stapfianus, a model desiccation-tolerant grass. Functional Plant Biology 36, 589–599.
Sporobolus stapfianus, a model desiccation-tolerant grass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotVegu7w%3D&md5=4ce0dbc4bc4765464abaa03a80cd5d4dCAS |

Gechev TS, Bergström E, Thomas-Oates J, Antonio C, Mueller-Roeber B, Schippers JHM, Fernie AR, Toneva V, Benina M, Obata T, Tohge T, Sujeeth N, Minkov I, Hille J, Temanni M-R, Marriott AS (2013) Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis. Cellular and Molecular Life Sciences 70, 689–709.
Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFektrs%3D&md5=353b6677c6b3c794350b11a09f3c6a84CAS | 22996258PubMed |

Georgieva K, Doncheva S, Mihailova G, Petkova S (2012) Response of sun- and shade-adapted plants of Haberlea rhodopensis to desiccation. Plant Growth Regulation 67, 121–132.
Response of sun- and shade-adapted plants of Haberlea rhodopensis to desiccation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xms1Wmt70%3D&md5=5f8ad23b11c183c1ba807dc9f955815cCAS |

Hallam ND, Luff SE (1980) Fine structural changes in the mesophyll tissue of the leaves of Xerophyta villosa during desiccation. Botanical Gazette 141, 173–179.
Fine structural changes in the mesophyll tissue of the leaves of Xerophyta villosa during desiccation.Crossref | GoogleScholarGoogle Scholar |

Heckathorn SA, DeLucia EH (1991) Effect of leaf rolling on gas exchange and leaf temperature of Andropogon gerardii and Spartina pectinata. Botanical Gazette 152, 263–268.
Effect of leaf rolling on gas exchange and leaf temperature of Andropogon gerardii and Spartina pectinata.Crossref | GoogleScholarGoogle Scholar |

Hendry GA, Grime JP (1993) ‘Methods in comparative plant ecology: a laboratory manual.’ (Springer: Dordrecht, The Netherlands)

Hoang TML, Williams B, Khanna H, Dale J, Mundree SG (2014) Physiological basis of salt stress tolerance in rice expressing the antiapoptotic gene SfIAP. Functional Plant Biology 41, 1168–1177.
Physiological basis of salt stress tolerance in rice expressing the antiapoptotic gene SfIAP.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1ymt7vK&md5=d758bacf846a42d6fefbf0ea58b80b07CAS |

Iljin WS (1957) Drought resistance in plants and physiological processes. Annual Review of Plant Physiology 8, 257–274.
Drought resistance in plants and physiological processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1cXmslWmsQ%3D%3D&md5=2abc036cc4848171360e758a5253831aCAS |

Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone. Plant Physiology 77, 483–485.
Extinction coefficients of chlorophyll a and b in N,N-dimethylformamide and 80% acetone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXht12jtrc%3D&md5=4365296c995bb32701e8f2b057898d42CAS | 16664080PubMed |

Kadioglu A, Terzi R, Saruhan N, Saglam A (2012) Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors. Plant Science 182, 42–48.
Current advances in the investigation of leaf rolling caused by biotic and abiotic stress factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFejurzM&md5=ea0a7f200d797a81ddef356d18f5ca52CAS | 22118614PubMed |

Liphschitz N, Waisel Y (1974) Existence of salt glands in various genera of the Gramineae. New Phytologist 73, 507–513.
Existence of salt glands in various genera of the Gramineae.Crossref | GoogleScholarGoogle Scholar |

Long SP (1999) Environmental responses. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 215–249. (Academic Press: San Diego, CA, USA)

Markovska Y, Tsonev T, Kimenov G (1997) Regulation of CAM and respiratory recycling by water supply in higher poikilohydric plants – Haberlea rhodopensis Friv. and Ramonda serbica Panč, at transition from biosis to anabiosis and vice versa. Botanica Acta 110, 18–24.
Regulation of CAM and respiratory recycling by water supply in higher poikilohydric plants – Haberlea rhodopensis Friv. and Ramonda serbica Panč, at transition from biosis to anabiosis and vice versa.Crossref | GoogleScholarGoogle Scholar |

Michaillat L, Mayer A (2013) Identification of genes affecting vacuole membrane fragmentation in Saccharomyces cerevisiae. PLoS One 8, e54160
Identification of genes affecting vacuole membrane fragmentation in Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXivVOksrg%3D&md5=7e333292ce0dd33a41f1b21db6d4c047CAS | 23383298PubMed |

Moore J, Nguema-Ona E, Vicré-Gibouin M, Sørensen I, Willats WT, Driouich A, Farrant J (2013) Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation. Planta 237, 739–754.
Arabinose-rich polymers as an evolutionary strategy to plasticize resurrection plant cell walls against desiccation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtVWqt7g%3D&md5=b1d26851596eba2ba6d1a06f9b2f35afCAS | 23117392PubMed |

Mundree SG, Farrant JM (2000) Some physiological and molecular insights into the mechanisms of desiccation tolerance in the resurrection plant Xerophyta viscosa Baker. In ‘Plant tolerance to abiotic stresses in agriculture: role of genetic engineering’. pp. 201–222. (Springer: Dordrecht, The Netherlands)

Mundree SG, Baker B, Mowla S, Peters S, Marais S, Willigen CV, Govender K, Maredza A, Muyanga S, Farrant JM, Thomson JA (2002) Physiological and molecular insights into drought tolerance. African Journal of Biotechnology 1, 28–38.
Physiological and molecular insights into drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvFGiug%3D%3D&md5=b3f7bf54a0c69c3cae13ab22aafd18b8CAS |

O’Toole JC, Cruz RT (1980) Response of leaf water potential, stomatal resistance, and leaf rolling to water stress. Plant Physiology 65, 428–432.
Response of leaf water potential, stomatal resistance, and leaf rolling to water stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhtlertg%3D%3D&md5=0ed3482208511da0f4633d46b935ceffCAS | 16661206PubMed |

Oliver MJ, Bewley JD (1997) Desiccation-tolerance of plant tissues: a mechanistic overview. In ‘Horticultural reviews’. pp. 171–213. (John Wiley & Sons Inc.: New York)

Oliver MJ, Tuba Z, Mishler BD (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecology 151, 85–100.
The evolution of vegetative desiccation tolerance in land plants.Crossref | GoogleScholarGoogle Scholar |

Oliver M, Cushman J, Koster K (2010) Dehydration tolerance in plants. In ‘Plant stress tolerance. Vol. 639’. (Ed. R Sunkar) pp. 3–24. (Humana Press: New York)

Orchard E, Wilson A (2005) Flora of Australia. In ‘Poaceae.’ (Eds K Mallett, TD Macfarlane) (Australian Biological Resources Study, CSIRO: Canberra)

Prendergast H, Hattersley P (1987) Australian C4 grasses (Poaceae) – leaf blade anatomical features in relation to C4 acid decarboxylation types. Australian Journal of Botany 35, 355–382.
Australian C4 grasses (Poaceae) – leaf blade anatomical features in relation to C4 acid decarboxylation types.Crossref | GoogleScholarGoogle Scholar |

Ristic Z, Jenks MA (2002) Leaf cuticle and water loss in maize lines differing in dehydration avoidance. Journal of Plant Physiology 159, 645–651.
Leaf cuticle and water loss in maize lines differing in dehydration avoidance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVCrurk%3D&md5=af1986945ef32bf5193934c4c58aa006CAS |

Rodriguez MCS, Edsgärd D, Hussain SS, Alquezar D, Rasmussen M, Gilbert T, Nielsen BH, Bartels D, Mundy J (2010) Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. The Plant Journal 63, 212–228.
Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpslymsr0%3D&md5=0de43d24c6c045bbd02152a9cc79b355CAS |

Rolny N, Costa L, Carrión C, Guiamet JJ (2011) Is the electrolyte leakage assay an unequivocal test of membrane deterioration during leaf senescence? Plant Physiology and Biochemistry 49, 1220–1227.
Is the electrolyte leakage assay an unequivocal test of membrane deterioration during leaf senescence?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1ags7rM&md5=ea0944ec73e45c54b76e51bc9281b113CAS | 21782462PubMed |

Rúgolo de Agrasar ZE, Vega AS (2004) Tripogon nicorae, a new species and synopsis of Tripogon (Poaceae: Chloridoideae) in America. Systematic Botany 29, 874–882.
Tripogon nicorae, a new species and synopsis of Tripogon (Poaceae: Chloridoideae) in America.Crossref | GoogleScholarGoogle Scholar |

Sherwin H, Farrant J (1998) Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa. Plant Growth Regulation 24, 203–210.
Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlOrsLY%3D&md5=08fb812e7e7b069909e4a7b71fe3fa11CAS |

Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytologist 125, 27–58.
The role of active oxygen in the response of plants to water deficit and desiccation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFams70%3D&md5=bbe41495b2c3bcce78882c992d144ae2CAS |

Tipping C, Murray DR (1999) Effects of elevated atmospheric CO2 concentration on leaf anatomy and morphology in Panicum species representing different photosynthetic modes. International Journal of Plant Sciences 160, 1063–1073.
Effects of elevated atmospheric CO2 concentration on leaf anatomy and morphology in Panicum species representing different photosynthetic modes.Crossref | GoogleScholarGoogle Scholar | 10568773PubMed |

Tuba Z, Lichtenthaler HK, Csintalan Z, Nagy Z, Szente K (1996) Loss of chlorophylls, cessation of photosynthetic CO2 assimilation and respiration in the poikilochlorophyllous plant Xerophyta scabrida during desiccation. Physiologia Plantarum 96, 383–388.
Loss of chlorophylls, cessation of photosynthetic CO2 assimilation and respiration in the poikilochlorophyllous plant Xerophyta scabrida during desiccation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XivV2qtrY%3D&md5=5340519bedf5eb7cae49820d203baaebCAS |

Tuba Z, Protor CF, Csintalan Z (1998) Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective. Plant Growth Regulation 24, 211–217.
Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitlOrsLc%3D&md5=661a20273798bd14f476cf46d1cceb4fCAS |

Turgut R, Kadioglu A (1998) The effect of drought, temperature and irradiation on leaf rolling in Ctenanthe setosa. Biologia Plantarum 41, 629–633.
The effect of drought, temperature and irradiation on leaf rolling in Ctenanthe setosa.Crossref | GoogleScholarGoogle Scholar |

Turner N (1981) Techniques and experimental approaches for the measurement of plant water status. Plant and Soil 58, 339–366.
Techniques and experimental approaches for the measurement of plant water status.Crossref | GoogleScholarGoogle Scholar |

Vander Willigen C, Pammenter NW, Mundree SG, Farrant JM (2004) Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP 3;1 and/or compartmentalization of subcellular components and metabolites play a role? Journal of Experimental Botany 55, 651–661.
Mechanical stabilization of desiccated vegetative tissues of the resurrection grass Eragrostis nindensis: does a TIP 3;1 and/or compartmentalization of subcellular components and metabolites play a role?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvFSrurs%3D&md5=1d0a6b6fd65459209a55ce200ac3df40CAS | 14966222PubMed |

Vertucci CW, Farrant JM (1995) Acquisition and loss of desiccation tolerance. In ‘Seed development and germination’. (Eds J Kigel, G Galili) pp. 237–271. (Marcel Dekker: New York)

Watson L, Dallwitz MJ (1992) The grass genera of the world. Version: 2nd April 2015. Available at http://delta-intkey.com/grass/www/tripogon.htm [Verified 30 November 2015]

Whittaker A, Martinelli T, Bochicchio A, Vazzana C, Farrant J (2004) Comparison of sucrose metabolism during the rehydration of desiccation‐ tolerant and desiccation‐sensitve leaf material of Sporobolus stapfianus. Physiologia Plantarum 122, 11–20.
Comparison of sucrose metabolism during the rehydration of desiccation‐ tolerant and desiccation‐sensitve leaf material of Sporobolus stapfianus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFehtrc%3D&md5=811bf154bdf1bbdff83e4b0e923e7920CAS |

Woodenberg WR, Pammenter N, Farrant JM, Driouich A, Berjak P (2014) Embryo cell wall properties in relation to development and desiccation in the recalcitrant-seeded Encephalartos natalensis (Zamiaceae) Dyer and Verdoorn. Protoplasma 252, 245–258.
Embryo cell wall properties in relation to development and desiccation in the recalcitrant-seeded Encephalartos natalensis (Zamiaceae) Dyer and Verdoorn.Crossref | GoogleScholarGoogle Scholar | 25015529PubMed |