Cryo-scanning electron microscopy (CSEM) in the advancement of functional plant biology. Morphological and anatomical applications
Margaret E. McCully A D , Martin J. Canny B and Cheng X. Huang CA Division of Plant Industry, CSIRO, Canberra, ACT 2601, Australia.
B Functional Ecology Group, Research School of Biological Sciences, Australian National University, Canberra, ACT 0200, Australia.
C Electron Microscopy Unit, Research School of Biological Sciences, Australian National University, Canberra, ACT 0200, Australia.
D Corresponding author. Email: margaret.mccully@csiro.au
Functional Plant Biology 36(2) 97-124 https://doi.org/10.1071/FP08304
Submitted: 27 November 2008 Accepted: 15 December 2008 Published: 5 February 2009
Abstract
Cryo-scanning electron microscopy (CSEM) is reviewed by exploring how the images obtained have changed paradigms of plant functions and interactions with their environment. Its power to arrest and stabilise plant parts in milliseconds, and to preserve them at full hydration for examination at micrometre resolution has changed many views of plant function. For example, it provides the only feasible way of accurately measuring stomatal aperture during active transpiration, and volume and shape changes in guard cells, or examining the contents of laticifers. It has revealed that many xylem conduits contain gas, not liquid, during the day, and that they can be refilled with sap and resume water transport. It has elucidated the management of ice to prevent cell damage in frost tolerant plants and has revealed for the first time inherent biological and physical features of root/soil interactions in the field. CSEM is increasingly used to reveal complementary structural information in studies of metabolism, fungal infection and symbiosis, molecular and genetic analysis.
Additional keywords: biopores, cryo-fixation, cryo-planing, cut flowers, desiccated tissues, exudation of liquids, food microscopy, frost resistance, fungal infection, hydrated tissues, intercellular spaces, laticifers, lichen water content, mucilage phase change, mycorrhizas, naturally frozen tissues, pathogenic fungi, pit membranes, resin canals, rhizosheath, rhizosphere, roots in soil, soil fauna, spittle bugs, stomatal aperture, surface wax structure, symbiotic fungi, tyloses, vessel lining, xylem embolism.
Acknowledgements
We thank the many researchers and journals who have freely provided us with micrographs or given permission to reproduce published images, and the referees for very helpful comments.
Abeysekera RM, McCully ME
(1993) The epidermal surface of the maize root tip. II. Abnormalities in a mutant which grows crookedly through soil. New Phytologist 125, 801–811.
| Crossref | GoogleScholarGoogle Scholar |
Abeysekera RM, McCully ME
(1994) The epidermal surface of the maize root tip. III. Isolation of the surface and characterization of some of its structural and mechanical properties. New Phytologist 127, 321–333.
| Crossref | GoogleScholarGoogle Scholar |
Albrechtová JTP,
Dueggelin M,
Duerrenberger M, Wagner E
(2004) Changes in the geometry of the apical meristem and concomitant changes in cell wall properties during photoperiodic induction of flowering in Chenopodium rubrum. New Phytologist 163, 263–269.
| Crossref | GoogleScholarGoogle Scholar |
Alexander C,
Jones D, McHardy WJ
(1987) Scanning electron microscopy of cryofixed mycorrhizas of Sitka spruce, Picea sitchensis (Bong.) Carr.: a comparison with critical point-dried material. New Phytologist 105, 613–617.
| Crossref | GoogleScholarGoogle Scholar |
Andersen PC,
Brodbeck BV, Mizell RF
(1992) Feeding by the leafhopper, Homalodisca coagulata, in relation to xylem fluid chemistry and tension. Journal of Insect Physiology 38, 611–622.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Apoga D, Jansson H-B
(2000) Visualization and characterization of the extracellular matrix of Bipolaris sorokiniana. Mycological Research 104, 564–575.
| Crossref | GoogleScholarGoogle Scholar |
Ashworth EN,
Echlin P,
Pearce RS, Hayes TL
(1988) Ice formation and tissue-response in apple twigs. Plant, Cell & Environment 11, 703–710.
| Crossref | GoogleScholarGoogle Scholar |
Ball MC,
Canny MJ,
Huang CX,
Egerton JJG, Wolfe J
(2006) Freeze/thaw-induced embolism depends on nadir temperature: the heterogeneous hydration hypothesis. Plant, Cell & Environment 29, 729–745.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bargel H,
Koch K,
Cerman Z, Neinhuis C
(2006) Structure–function relationships of the plant cuticle and cuticular waxes – a smart material? Functional Plant Biology 33, 893–910.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Barker WW,
Welch SA,
Chu S, Banfield JF
(1998) Experimental observations of the effects of bacteria on aluminosilicate weathering. The American Mineralogist 83, 1551–1563.
|
CAS |
Berndt ML,
McCully ME, Canny MJ
(1999) Is xylem embolism and refilling involved in the rapid wilting and recovery of plants following root cooling and rewarming? A cryo-microscope investigation. Plant Biology 1, 506–515.
| Crossref | GoogleScholarGoogle Scholar |
Braun EJ, Howard RJ
(1994) Adhesion of fungal spores and germlings to host plant surfaces. Protoplasma 181, 202–212.
| Crossref | GoogleScholarGoogle Scholar |
Buchard C,
McCully ME, Canny MJ
(1999) Daily embolism and refilling of root xylem vessels in three dicotyledonous crop plants. Agronomie 19, 97–106.
| Crossref | GoogleScholarGoogle Scholar |
Burn JE,
Hocart CH,
Birch RJ,
Cork AC, Williamson RE
(2002) Functional analysis of the cellulose synthase genes CesA1, CesA2, and CesA3 in Arabidopsis. Plant Physiology 129, 797–807.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Burton RA,
Gibeaut DM,
Bacic A,
Findlay K,
Roberts K,
Hamilton A,
Baulcombe DC, Fincher GB
(2000) Virus-induced silencing of a plant cellulose synthase gene. The Plant Cell 12, 691–704.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Campbell R, Porter R
(1982) Low-temperature scanning electron microscopy of micro-organisms in soil. Soil Biology & Biochemistry 14, 241–245.
| Crossref | GoogleScholarGoogle Scholar |
Canny MJ
(1997a) Vessel contents of leaves after excision – a test of Scholander’s assumption. American Journal of Botany 84, 1217–1222.
| Crossref | GoogleScholarGoogle Scholar |
Canny MJ
(1997b) Vessel contents during transpiration-embolisms and refilling. American Journal of Botany 84, 1223–1230.
| Crossref | GoogleScholarGoogle Scholar |
Canny MJ
(1997c) Tyloses and the maintenance of transpiration. Annals of Botany 80, 565–570.
| Crossref | GoogleScholarGoogle Scholar |
Canny MJ
(2001) Embolisms and refilling in the maize leaf lamina, and the role of the protoxylem cavity. American Journal of Botany 88, 47–51.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Canny MJ, Huang CX
(1993) What is in the intercellular spaces of roots? Evidence from the cryo-analytical-scanning electron microscope. Physiologia Plantarum 87, 561–568.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Canny MJ, Huang CX
(2006) Leaf water content and palisade cell size. New Phytologist 170, 75–85.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Canny MJ,
Sparks JP,
Huang CX, Roderick ML
(2007) Air embolisms exsolving in the transpiration water – the effect of constrictions in the xylem pipes. Functional Plant Biology 34, 95–111.
| Crossref | GoogleScholarGoogle Scholar |
Chaudhury AM,
Ming L,
Miller C,
Craig S,
Dennis ES, Peacock WJ
(1997) Fertilization-independent seed development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 94, 4223–4228.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chaudhury AM,
Craig S,
Dennis ES, Peacock WJ
(1998) Ovule and embryo development, apomixis and fertilization. Current Opinion in Plant Biology 1, 26–31.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chenu C,
Hassink J, Bloem J
(2001) Short-term changes in the spatial distribution of microorganisms in soil aggregates as affected by glucose addition. Biology and Fertility of Soils 34, 349–356.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Choat B,
Ball M,
Luly J, Holtum J
(2003) Pit membrane porosity and water stress-induced cavitation in four co-existing dry rainforest tree species. Plant Physiology 131, 41–48.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cobb AR,
Choat B, Holbrook NM
(2007) Dynamics of freeze-thaw embolism in Smilax rotundifolia (Smilacaceae). American Journal of Botany 94, 640–649.
| Crossref | GoogleScholarGoogle Scholar |
Cochard H,
Bodet C,
Améglio T, Cruizat P
(2000) Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or artifacts? Plant Physiology 124, 1191–1202.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cochard H,
Froux F,
Mayr S, Coutand C
(2004) Xylem wall collapse in water-stressed pine needles. Plant Physiology 134, 401–408.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Craig S, Beaton CD
(1996) A simple cryo-SEM method for delicate plant tissues. Journal of Microscopy 182, 102–105.
| Crossref | GoogleScholarGoogle Scholar |
Craven LA,
Miller C, White RG
(2006) A new name, and notes on extra-floral nectaries, in Lagunaria (Malvaceae, Malvoideae). Blumea 51, 345–353.
Crews LJ,
McCully ME, Canny MJ
(1998) Xylem feeding by spittlebug nymphs: some observations by optical and cryo-scanning electron microscopy. American Journal of Botany 85, 449–460.
| Crossref | GoogleScholarGoogle Scholar |
Crews LJ,
McCully ME, Canny MJ
(2003) Mucilage production by wounded xylem tissue of maize roots – time course and stimulus. Functional Plant Biology 30, 755–766.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Czarnota MA,
Paul RN,
Dayan FE,
Nimbal CI, Weston LA
(2001) Mode of action, localization of production, chemical nature, and activity of sorgoleone: a potent PSII inhibitor in Sorghum spp. exudates. Weed Technology 15, 813–825.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
da Silva EAA,
Toorop PE,
van Aelst AC, Hilhorst HWM
(2004) Abscisic acid controls embryo growth potential and endosperm cap weakening during coffee (Caffea arabica cv. Rubi) seed germination. Planta 220, 251–261.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
da Silva EAA,
de Melo DLB,
Davide AC,
de Bode N,
Abreu GB,
Faria JMR, Hilhorst HWM
(2007) Germination ecophysiology of Annona crassiflora seeds. Annals of Botany 99, 823–830.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
da Silva EAA,
Toorop PE,
Van Lammeren AAM, Hilhorst HWM
(2008) ABA inhibits embryo cell expansion and early cell division events during coffee (Coffea arabica ‘Rubi’) seed germination. Annals of Botany 102, 425–433.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dell B, Wallace IM
(1981) Surface root system of Eucalyptus marginate Sm: anatomy of non-mycorrhizal roots. Australian Journal of Botany 29, 565–577.
| Crossref | GoogleScholarGoogle Scholar |
Dijksterhuis J,
van Driel KGA,
Sanders MG,
Molenaar D,
Houbraken JAMP,
Samson RA, Kets EPW
(2002) Trehalose degradation and glucose efflux precede cell ejection during germination of heat-resistant ascospores of Talaromyces macrosporus. Archives of Microbiology 178, 1–7.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dijksterhuis J,
Nijsse J,
Hoekstra FA, Golovina EA
(2007) High viscosity and anisotropy characterize the cytoplasm of fungal dormant stress-resistant spores. Eukaryotic Cell 6, 157–170.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Dong Z,
Canny MJ,
McCully ME,
Roboredo MR,
Cabadilla CF,
Ortega E, Rodés R
(1994) A nitrogen-fixing endophyte of sugarcane stems: a new role for the apoplast. Plant Physiology 105, 1139–1147.
|
CAS |
PubMed |
Dorioz JM,
Robert M, Chenu C
(1993) The role of roots fungi and bacteria on clay particle organization. An experimental approach. Geoderma 56, 179–194.
| Crossref | GoogleScholarGoogle Scholar |
Dragota S, Riederer M
(2007) Epicuticular wax crystals of Wollemia nobilis: morphology and chemical composition. Annals of Botany 100, 225–231.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Duncan KE, Howard RJ
(2000) Cytological analysis of wheat infection by the leaf blotch pathogen Mycosphaerella graminicola. Mycological Research 104, 1074–1082.
| Crossref | GoogleScholarGoogle Scholar |
England WE,
McCully ME, Huang CX
(1997) Solvent vapour lock: an extreme case of the problem caused by lignified and suberized cell walls during resin infiltration. Journal of Microscopy 185, 85–93.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Facette MR,
Canny MJ, McCully ME
(2001) Measurements of the time to refill embolized vessels. Plant Physiology and Biochemistry 39, 59–66.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Fomina M,
Charnock JM,
Hillier S,
Alvarez R,
Livens F, Gadd GM
(2008) Role of fungi in the biogeochemical fate of depleted uranium. Current Biology 18, R375–R377.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Franks PJ, Farquhar GD
(2007) The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiology 143, 78–87.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fyson A,
Kerr P,
Lott JNA, Oaks A
(1988) The structure of the rhizosphere of maize seedling roots: a cryogenic scanning electron microscopy study. Canadian Journal of Botany 66, 2431–2435.
García-Segovia P,
Andrés-Bello A, Martínez-Monzó J
(2008) Textural properties of potatoes (Solanum tuberosum L., cv. Monalisa) as affected by different cooking practices. Journal of Food Engineering 88, 28–35.
| Crossref | GoogleScholarGoogle Scholar |
van Gardingen PR,
Jeffree CE, Grace J
(1989) Variation in stomatal aperture in leaves of Avena fatua L. observed by low-temperature scanning electron microscopy. Plant, Cell & Environment 12, 887–898.
| Crossref | GoogleScholarGoogle Scholar |
van Gardingen PR,
Grace J, Jeffree CE
(1991) Abrasive damage by wind to the needle surfaces of Picea sitchensis (Bong.) Carr. And Pinus sylvestris L. Plant, Cell & Environment 14, 185–193.
| Crossref | GoogleScholarGoogle Scholar |
Gebbie LK,
Burn JE,
Hocart CH, Williamson RE
(2005) Genes encoding ADP-ribosylation factors in Arabidopsis thaliana (L.) Heynh.; genome analysis and antisense suppression. Journal of Experimental Botany 56, 1079–1091.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gochnauer MB,
McCully ME, Labbé H
(1989) Different populations of bacteria associated with sheathed and bare regions of roots of field-grown maize. Plant and Soil 114, 107–120.
| Crossref | GoogleScholarGoogle Scholar |
Golovina EA,
Hoekstra FA, Van Aelst AC
(2001) The competence to acquire cellular desiccation tolerance is independent of seed morphological development. Journal of Experimental Botany 52, 1015–1027.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Guggenheim R,
Düggelin M,
Mathys D, Grabski C
(1991) Low-temperature SEM for detection of fungicide activity. Journal of Microscopy 16, 337–342.
Guinel FC, McCully ME
(1986) Some water-related physical properties of maize root-cap mucilage. Plant, Cell & Environment 9, 657–666.
| Crossref | GoogleScholarGoogle Scholar |
Hall DE,
MacGregor KB,
Nijsse J, Bown AW
(2004) Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. European Journal of Plant Pathology 110, 441–447.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Hawes MC,
Gunawardena U,
Miyasaka S, Zhao X
(2000) The role of border cells in plant defence. Trends in Plant Science 5, 128–133.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hinsinger P,
Gobran GR,
Gregory PJ, Wenzel WW
(2005) Rhizosphere geometry and heterogeneity arising from root-mediated physical and chemical processes. New Phytologist 168, 293–303.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hoad SP,
Marzoli A,
Grace J, Jeffree CE
(1998) Response of leaf surfaces and gas exchange to wind stress and acid mist in birch (Betula pubescens). Trees 13, 1–12.
Honegger R, Peter M
(1994) Routes of solute translocation and the location of water in heteromerous lichens visualized with cryotechniques in light and electron microscopy. Symbiosis 16, 167–186.
Huang CX,
Canny MJ,
Oates K, McCully ME
(1994) Planing frozen hydrated plant specimens for SEM observation and EDX analysis. Microscopy Research and Technique 28, 67–74.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hukin D,
Cochard H,
Dreyer E,
Le Thiec D, Bogeat-Triboulot MB
(2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? Journal of Experimental Botany 56, 2003–2010.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Iijima M,
Sako Y, Rao TP
(2003) A new approach for the quantification of root-cap mucilage exudation in the soil. Plant and Soil 255, 399–407.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jahromi FG,
Cother EJ, Ash GJ
(2002) Early infection process of Damasonium minus by the potential mycoherbistat Rhynchosporium alismatis. Canadian Journal of Plant Pathology 24, 131–136.
Jansen S,
Pletsers A, Sano Y
(2008) The effect of preparation techniques on SEM-imaging of pit membranes. IAWA Journal 29, 161–178.
Janson J,
Reinders MC,
Valkering AGM,
Van Tuyl JM, Keijzer CJ
(1994) Pistil exudate production and pollen tube growth in Lilium longiflorum Thunb. Annals of Botany 73, 437–446.
| Crossref | GoogleScholarGoogle Scholar |
Jansson H-B, Åkesson H
(2003) Extracellular matrix, esterase and the phytotoxin +++prehelminthosporol in infection of barley leaves by Bipolaris sorokiniana. Journal of Plant Pathology 109, 599–605.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Jansson H-B,
Persson C, Odeslius R
(2000) Growth and capture activities of nematophagous fungi in soil visualized by low temperature scanning electron microscopy. Mycologia 92, 10–15.
| Crossref | GoogleScholarGoogle Scholar |
Jennessen J,
Schnürer J,
Olsson J,
Samson RA, Dijksterhuis J
(2008) Morphological characteristics of sporangiospores of the tempe fungus Rhizopus oligosporus differentiate it from other tax a of the R. microsporus group. Mycological Research 112, 547–563.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kalinganire A,
Harwood CE,
Slee MU, Simons AJ
(2000) Floral structure, stigma receptivity and pollen viability in relation to protandry and self-incompatibility in silky oak (Grevillea robusta A. Cunn.). Annals of Botany 86, 133–148.
| Crossref | GoogleScholarGoogle Scholar |
Kaminskyj SGW, Dahms TES
(2008) High spatial resolution surface imaging and analysis of fungal cells using SEM and AFM. Micron (Oxford, England) 39, 349–361.
|
CAS |
Keijzer CJ,
Leferink-Ten Klooster HB, Reinders MC
(1996) The mechanics of the grass flower: anther dehiscence and pollen shedding in maize. Annals of Botany 78, 15–21.
| Crossref |
Kirkegaard J,
Christen O,
Krupinsky J, Layzell D
(2008) Break crop benefits in temperate wheat production. Field Crops Research 107, 185–195.
| Crossref | GoogleScholarGoogle Scholar |
Klein E,
Bar E,
Forni C,
Malkins S, Tel-Or E
(1992) The application of cryo-SEM techniques to the study of the symbiotic association in the Azolla leaf cavity. Journal of Microscopy 167, 273–278.
Koller D, Zamski E
(2002) The phototropic pulvinus of bean Phaseolus vulgaris L. functional features. Plant Biology 4, 584–594.
| Crossref | GoogleScholarGoogle Scholar |
Kuroda K,
Ohtani J, Fujikawa S
(1997) Supercooling of xylem parenchyma cells in tropical and subtropical hardwood species. Trees (Berlin) 12, 97–106.
| Crossref |
Lanoiselet V,
Cother EJ,
Ash G, van de Ven R
(2001) Production, germination and infectivity of chlamydospores of Rhynchosporium alismatis. Mycological Research 105, 441–446.
| Crossref | GoogleScholarGoogle Scholar |
Laüchli A,
James RA,
Huang CX,
McCully ME, Munns R
(2008) Cell-specific localization of Na+ in roots of durum wheat and possible control points for salt exclusion. Plant, Cell & Environment 31, 1565–1574.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Lovell D,
Wu L,
White R,
Machado A,
Llewellyn DJ,
Dennis ES, Anderssen RS
(2007) Phenotyping cotton ovule fibre initiation with spatial statistics. Australian Journal of Botany 55, 608–617.
| Crossref | GoogleScholarGoogle Scholar |
Maldonado R,
Molina-Garcia AD,
Sanchez-Ballesta MT,
Escribano MI, Merodio C
(2002) High CO2 atmosphere modulating the phenolic response associated with cell adhesion and hardening of Annona cherimola fruit stored at chilling temperature. Journal of Agricultural and Food Chemistry 50, 7564–7569.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Martin-Diana AB,
Rico D,
Frías J,
Henehan GTM,
Mulcahy J,
Barat JM, Barry-Ryan C
(2006) Effect of calcium lactate and heat-shock on texture in fresh-cut lettuce in storage. Journal of Food Engineering 77, 1069–1077.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Massicotte HB,
Melville LH, Peterson RL
(1987) Scanning microscopy of ectomycorrhizae. Potential and limitations. Scanning Microscopy l, 1439–1454.
Mayr S,
Cochard H,
Améglio T, Kikuta SB
(2007) Embolism formation during freezing in the wood of Picea abies. Plant Physiology 143, 60–67.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McCully ME
(1994) Accumulation of high levels of potassium in the developing xylem of soybean and some other dicotyledons. Protoplasma 183, 116–125.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME
(1995) Water efflux from the surface of field-grown grass roots. Observations by cryo-scanning electron microscopy. Physiologia Plantarum 95, 217–224.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME
(1999a) Root xylem embolisms and refilling. Relation to water potentials of soil, roots, and leaves, and osmotic potentials of root xylem sap. Plant Physiology 119, 1001–1008.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McCully ME
(1999b) Roots in soil. Unearthing the complexities of roots and their rhizospheres. Annual Review of Plant Physiology and Plant Molecular Biology 50, 695–718.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McCully ME
(2004) Lucerne drilling rigs improve duplex soils. Farming Ahead 153, 45–46.
McCully ME
(2007) Rhizosphere allelopathy. Allelopathy Journal 19, 75–84.
McCully ME, Boyer JS
(1997) The expansion of maize root-cap mucilage during hydration 3. Changes in water potential and water content. Physiologia Plantarum 99, 169–177.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME, Canny MJ
(1988) Pathways and processes in water and nutrient movement in roots. Plant and Soil 111, 159–170.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME, Canny MJ
(1994) Contributions of the surface of the root-tip to the growth of Zea roots in the soil. Plant and Soil 165, 315–321.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME, Sealey LJ
(1996) The expansion of maize root-cap mucilage during hydration. 2. Observations on soil-grown roots by cryo-scanning electron microscopy. Physiologia Plantarum 97, 454–462.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME,
Canny MJ, Van Steveninck RFM
(1987) Accumulation of potassium by differentiating metaxylem elements of maize roots. Physiologia Plantarum 69, 73–80.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
McCully ME,
Huang CX, Ling JEC
(1998) Daily embolism and refilling of xylem vessels in the roots of field-grown maize. New Phytologist 138, 327–342.
| Crossref | GoogleScholarGoogle Scholar |
McCully ME,
Shane MW,
Baker AN,
Huang CX,
Ling LEC, Canny MJ
(2000) The reliability of cryoSEM for the observation and quantification of xylem embolisms and quantitative analysis of xylem sap in situ. Journal of Microscopy 198, 24–33.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McCully ME,
Canny MJ, Huang CX
(2004) The management of extracellular ice by petioles of frost-resistant herbaceous plants. Annals of Botany 94, 665–674.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
McCully ME,
Miller C,
Sprague SJ,
Huang CX, Kirkegaard JA
(2008) Distribution of glucosinolates and sulphur-rich cells in roots of field-grown canola (Brassica napus). New Phytologist 180, 193–205.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Melcher PJ,
Goldstein G,
Meinzer FC,
Yount DE,
Jones TJ,
Holbrook NM, Huang CX
(2001) Water relations of coastal and estuarine Rhizophora mangle: xylem pressure potential and dynamics of embolism formation and repair. Oecologia 126, 182–192.
| Crossref | GoogleScholarGoogle Scholar |
Mersey B, McCully ME
(1978) Monitoring the course of fixation of plant cells. Journal of Microscopy 114, 49–76.
Mommer L,
Pons TL,
Wolters-Arts M,
Venema JH, Visser EJW
(2005) Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance. Plant Physiology 139, 497–508.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nell TA, Clark DG
(2001) Quantification of emboli by visualization of air filled xylem vessels. Acta Horticulturae 543, 245–250.
Neya O,
Golovina EA,
Nijsse J, Hoekstra FA
(2004) Ageing increases the sensitivity of neem (Azadirachta indica) seeds to imbibitional stress. Seed Science Research 14, 205–217.
| Crossref | GoogleScholarGoogle Scholar |
Nijsse J, Put HMC
(2007) Cryo-planing for cryo-scanning electron microscopy (SEM) – A method for observation of xylem contents in Rosa stems. Acta Horticulturae 751, 487–491.
Nijsse J, Van Aelst AC
(1999) Cryo-planing for cryo-scanning electron microscopy. Scanning 21, 372–378.
|
CAS |
PubMed |
Nijsse J,
Erbe E,
Brantjes NBM,
Schel JHN, Wergin WP
(1998) Low-temperature scanning electron microscopic observations on endosperm in imbibed and germinated lettuce seeds. Canadian Journal of Botany 76, 509–516.
| Crossref | GoogleScholarGoogle Scholar |
Nijsse J,
van Meeteren U, Keijzer CJ
(2000) Air in xylem vessels of cut flowers. Acta Horticulturae 517, 479–486.
Nijsse J,
van den Heijden GWAM,
van Leperen W,
Keijzer CJ, van Meeterem U
(2001) Xylem hydraulic conductivity related to conduit dimensions along chrysanthemum stems. Journal of Experimental Botany 52, 319–327.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Nijsse J,
Walther P, Hoekstra FA
(2004) Cold-induced imbibition damage of lettuce embryos: a study using cryo-scanning electron microscopy. Seed Science Research 14, 117–126.
| Crossref | GoogleScholarGoogle Scholar |
Pate JS, Canny MJ
(1999) Quantification of vessel embolisms by direct observation: a comparison of two methods. New Phytologist 141, 33–44.
| Crossref | GoogleScholarGoogle Scholar |
Pearce RS
(1988) Extracellular ice and cell shape in frost-stressed cereal leaves: a low temperature scanning-electron-microscopy study. Planta 175, 313–324.
| Crossref | GoogleScholarGoogle Scholar |
Pearce RS, Beckett A
(1987) Cell shape in leaves of drought-stressed barley examined by low temperature scanning electron microscopy. Annals of Botany 59, 191–195.
Pickard WF
(2008) Laticifers and secretory ducts: two other tube systems in plants. New Phytologist 177, 877–887.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Pighin JA,
Zheng H,
Balakshin LJ,
Goodman IP,
Western TL,
Jetter R,
Kunst L, Samuels AL
(2004) Plant cuticular lipid export requires an ABC transporter. Science 306, 702–704.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Prats E,
Gay AP,
Mur LAJ,
Thomas BJ, Carver TLW
(2006) Stomatal lock-open, a consequence of epidermal cell death, follows transient suppression of stomatal opening in barley attacked by Blumeria graminis. Journal of Experimental Botany 57, 2211–2226.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Prillieux E
(1869) Sur la formation de glaçons a l’intérieur des plantes. Annales des Sciences Naturelles 12, 125–134.
Quiles A,
Hernando I,
Pérez-Munuera I, Lluch MA
(2007) Effect of calcium propionate on the microstructure and pectin methylesterase activity in the parenchyma of fresh-cut Fuji apples. Journal of the Science of Food and Agriculture 87, 511–519.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Rauscher M,
Adám AL,
Wirtz S,
Guggenheim R,
Mendgen K, Deising HB
(1999) PR-1 protein inhibits the differentiation of rust infection hyphae in leaves of acquired resistant broad bean. The Plant Journal 19, 625–633.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Read ND, Lord KM
(1991) Examination of living fungal spores by scanning electron microscopy. Experimental Mycology 15, 132–139.
| Crossref | GoogleScholarGoogle Scholar |
Read ND,
Porter R, Beckett A
(1983) A comparison of preparative techniques for the examination of the external morphology of fungal material with the scanning electron microscope. Canadian Journal of Botany 61, 2059–2070.
Refshauge S,
Watt M,
McCully ME, Huang CX
(2006) Frozen in time: a new method using cryo-scanning electron microscopy to visualize root-fungal interactions. New Phytologist 172, 369–374.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Roberson EB,
Chenu C, Firestone MK
(1993) Microstructural changes in bacterial exopolysaccharides during desiccation. Soil Biology & Biochemistry 25, 1299–1301.
| Crossref | GoogleScholarGoogle Scholar |
Roca MG,
Arlt J,
Jeffree CE, Read ND
(2005) Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryotic Cell 4, 911–919.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Roden JS,
Canny MJ,
Huang X, Ball MC
(2009) Frost tolerance and ice formation in Pinus radiata needles: ice management by the endodermis and transfusion tissues. Functional Plant Biology 36, 180–189.
Roy S,
Babic I,
Watada AE, Wergin WP
(1996) Unique advantages of using low temperature scanning electron microscopy to observe bacteria. Protoplasma 195, 133–143.
| Crossref | GoogleScholarGoogle Scholar |
Rügner A,
Rumbolz J,
Huber B,
Bleyer G,
Gisi U,
Kassenmeyer H-H, Guggenheim R
(2002) Formation of overwintering structures of Uncinula necator and colonization of grapevine under field conditions. Plant Pathology 51, 322–330.
| Crossref | GoogleScholarGoogle Scholar |
Rumbolz J,
Wirtz S,
Kassemeyer H-H,
Guggenheim R,
Schäfer E, Büche C
(2002) Sporulation of Plasmopara viticola: differentiation and light regulation. Plant Biology 4, 413–422.
| Crossref | GoogleScholarGoogle Scholar |
Ryan MH,
McCully ME, Huang CX
(2003) Location and quantification of phosphorus and other elements in fully-hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytologist 160, 429–441.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Ryan MH,
McCully ME, Huang CX
(2007) Relative amounts of soluble and insoluble forms of phosphorus and other elements in intraradical hyphae and arbuscules of arbuscular mycorrhizas. Functional Plant Biology 34, 457–464.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Salvador A,
Arnal L,
Besada C,
Larrea V,
Quiles A, Pérez-Munuera I
(2007) Physiological and structural changes during ripening and deastringency treatment of persimmon fruit cv. ‘Rojo Brillante’. Postharvest Biology and Technology 46, 181–188.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Sargent JA
(1983) Cryopreservation of roots for scanning electron microscopy. Annals of Botany 58, 183–185.
Scheidegger C
(1994) Low-temperature scanning electron microscopy: the localization of free and perturbed water and its role in the morphology of the lichen symbionts. Cryptogamic Botany 4, 290–299.
Scheidegger C
(1995) Reproductive strategies in Vezdaea (Lecanorales, lichenized Ascomycetes): a low temperature scanning electron microscope study of a ruderal species. Cryptogamic Botany 5, 163–171.
Scheidegger C, Brunner I
(1993) Freeze-fracturing for low-temperature scanning electron microscopy of Hartig net in synthesized Picea abies – Hebeloma crustuliniforme and – Tricholoma vaccinum ectomycorrhizas. New Phytologist 123, 123–132.
Scheidegger C,
Günthardt-Goerg M,
Matyssek R, Hatvani P
(1991) Low-temperature scanning electron microscopy of birch leaves after exposure to ozone. Journal of Microscopy 161, 85–95.
|
CAS |
Scheidegger C,
Schroeter B, Frey B
(1995) Structural and functional processes during water vapour uptake and desiccation in selected lichens with green algal symbionts. Planta 197, 399–409.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Schijlen EGWM,
de Vos CHR,
Martens S,
Jonker HH,
Rosin FM,
Molthoff JW,
Tikunov YM,
Angenent GC,
van Tunen AJ, Bovy AG
(2007) RNA interference silencing of chalcone synthase, the first step in the flavonoid biosynthesis pathway, leads to parthenopcarpic tomato fruits. Plant Physiology 144, 1520–1530.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schroeter B, Scheidegger C
(1995) Water relations in lichens at subzero temperatures: structural changes and carbon dioxide exchange in the lichen Umbilicaria aprina from continental Antarctica. New Phytologist 131, 273–285.
| Crossref | GoogleScholarGoogle Scholar |
Servili M,
Minnocci A,
Veneziani G,
Taticchi A,
Urbani S,
Esposto S,
Sebastiani L,
Valmorri S, Corsetti A
(2008) Compositional and tissue modifications induced by the natural fermentation process in table olives. Journal of Agricultural and Food Chemistry 56, 6389–6396.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Shane MW,
McCully ME, Canny MJ
(2000a) Architecture of branch-root junctions in maize: Structure of the connecting xylem and the porosity of pit membranes. Annals of Botany 85, 613–624.
| Crossref | GoogleScholarGoogle Scholar |
Shane MW,
McCully ME, Canny MJ
(2000b) The vascular system of maize stems revisited: Implications for water transport and xylem safety. Annals of Botany 86, 245–258.
| Crossref | GoogleScholarGoogle Scholar |
Somasundaram S,
Fukuzono S, Iijima M
(2008) Dynamics of root border cells in rhizosphere soil of Zea mays L.: crushed cells during root penetration, survival in the soil, and long term soil compaction effect. Plant Production Science 11, 440–446.
| Crossref | GoogleScholarGoogle Scholar |
Souza-Egipsy V,
Valladares F, Ascaso C
(2000) Water distribution in foliose lichen species: Interactions between method of hydration, lichen substances and thallus anatomy. Annals of Botany 86, 595–601.
| Crossref | GoogleScholarGoogle Scholar |
Speransky VV,
Speransky SR, Brawley SH
(1999) Cryoanalytical studies of freezing damage and recovery in Fucus vesiculosus (Phaeophyceae). Journal of Phycology 35, 1264–1275.
| Crossref | GoogleScholarGoogle Scholar |
Speransky VV,
Brawley SH, McCully ME
(2001) Ion fluxes and modification of the extracellular matrix during gamete release in fucoid algae. Journal of Phycology 37, 555–573.
| Crossref | GoogleScholarGoogle Scholar |
St Aubin G,
Canny MJ, McCully ME
(1986) Living vessel elements in the late metaxylem of sheathed maize roots. Annals of Botany 58, 577–588.
Thomson WW, Platt KA
(1997) Conservation of cell order in desiccated mesophyll of Selaginella lepidophylla ([Hook and Grev.] Spring). Annals of Botany 79, 439–447.
| Crossref | GoogleScholarGoogle Scholar |
Tyree MT, Cochard H
(2003) Vessel contents of leaves after excision: a test of the Scholander assumption. Journal of Experimental Botany 54, 2133–2139.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tyree MT,
Salleo S,
Nardini A,
Lo Gullo MA, Mosca R
(1999) Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm? Plant Physiology 120, 11–21.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tyree MT,
Cochard H, Cruiziat P
(2003) The water-filled versus air-filled status of vessels cut open in air: the ‘Scholander assumption’ revisited. Plant, Cell & Environment 26, 613–621.
| Crossref | GoogleScholarGoogle Scholar |
Utsumi Y,
Sano Y,
Fujikawa S,
Funada R, Ohtani J
(1998) Visualization of cavitated vessels in winter and refilled vessels in spring in diffuse-porous trees by cryo-scanning eletron microscopy. Plant Physiology 117, 1463–1471.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Utsumi Y,
Sano Y,
Funda R,
Fujikawa S, Ohtani J
(1999) The progression of cavitation in earlywood vessels of Fraxinus mandshurica var. japonica during freeing and thawing. Plant Physiology 121, 897–904.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Utsumi Y,
Sano Y,
Funda R,
Ohtani J, Fujikawa S
(2003) Seasonal and perennial changes in the distribution of water in the sapwood of conifers in a sub-frigid zone. Plant Physiology 131, 1826–1833.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Valladares F,
Sancho LG, Ascaso C
(1998) Water storage in the lichen family Umbilicariaceae. Botanica Acta 111, 99–107.
Van Cauwenberghe O,
Newcomb W,
Canny MJ, Layzell DB
(1993) Dimensions and distribution of intercellular spaces in cryo-planed soybean nodules. Physiologia Plantarum 89, 252–261.
| Crossref | GoogleScholarGoogle Scholar |
Van der Weele CM,
Canny MJ, McCully ME
(1996) Water in aerenchyma spaces in roots. A fast diffusion path for solutes. Plant and Soil 184, 492–501.
Van Dongen JT,
Ammerlaan AMH,
Wouterlood M,
Van Aelst AAC, Borstlap AC
(2003) Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Annals of Botany 91, 729–737.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Van Ieperen W,
Nijsse J,
Keijzer CJ, Van Meeteren U
(2001) Induction of air embolism in xylem conduits of pre-defined diameter. Journal of Experimental Botany 52, 981–991.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Van Ieperen W,
Van Meeteren U, Nijsse J
(2002) Embolism repair in cut flower stems: a physical approach. Postharvest Biology and Technology 25, 1–14.
| Crossref | GoogleScholarGoogle Scholar |
Van Meeteren U,
van Gelder H, van Leperen W
(2000) Reconsideration of the use of deionized water as vase water in postharvest experiments on cut flowers. Postharvest Biology and Technology 18, 169–181.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Vander Willigen C,
Pammenter NW,
Jaffer MA,
Mundree SG, Farrant JM
(2003) An ultrastructural study using anhydrous fixation of Eragrostis nindensis, a resurrection grass with both desiccation-tolerant and – sensitive tissues. Functional Plant Biology 30, 281–290.
| Crossref | GoogleScholarGoogle Scholar |
Vartanian N,
Wertheimer DS, Couderc H
(1983) Scanning electron microscopic aspects of short tuberized roots, with special reference to cell rhizodermis evolution under drought and rehydration. Plant, Cell & Environment 6, 39–46.
Vermeer J, McCully ME
(1982) The rhizosphere in Zea: new insight into its structure and development. Planta 156, 45–61.
| Crossref | GoogleScholarGoogle Scholar |
Vögeli-Lange R,
Mohr U,
Wiemken A,
Düggelin M,
Guggenheim R, Boller T
(1995) Developmental regulation of susceptibility and tolerance to Fusarium root rot in beans. Botanica Acta 108, 387–395.
Voigt D, Gorb S
(2008) An insect trap as habitat: cohesion-failure mechanism prevents adhesion of Pameridea roridulae bugs to the sticky surface of the plant Roridula gorgonias. Journal of Experimental Biology 211, 2647–2657.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walther P, Müller M
(1999) Biological ultrastructure as revealed by high resolution cryo-SEM of block faces after cryo-sectioning. Journal of Microscopy 196, 279–287.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wang Y,
Chen Y,
Lavin C, Gretz MR
(2000) Extracellular matrix assembly in diatoms (Bacillariophyceae). IV. Ultrastructure of Achnanthes longipes and Cymbella cistula as revealed by high-pressure freezing/freeze substitution and cryo-field emission scanning electron microscopy. Journal of Phycology 36, 367–378.
| Crossref | GoogleScholarGoogle Scholar |
Watt M,
McCully ME, Jeffree CE
(1993) Plant and bacterial mucilages of the maize rhizosphere: comparison of their soil binding properties and histochemistry in a model system. Plant and Soil 151, 151–165.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Watt M,
McCully ME, Canny MJ
(1994) Formation and stabilization of rhizosheaths of Zea mays L. Effect of soil water content. Plant Physiology 106, 179–186.
|
CAS |
PubMed |
Watt M,
Kirkegaard JA, Rebetzke GJ
(2005) A wheat genotype developed for rapid leaf growth copes well with the physical and biological constraints of unploughed soil. Functional Plant Biology 32, 695–706.
| Crossref | GoogleScholarGoogle Scholar |
Watt M,
Silk WK, Passioura JB
(2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Annals of Botany 97, 839–855.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Watt M,
Magee LJ, McCully ME
(2008) Types, structure and potential for axial water flow in the deepest roots of field-grown cereals. New Phytologist 178, 135–146.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Weisbach C,
Walther P,
Hartwig UA, Nosberger J
(1999) Electron microscopic investigation of water occlusions in intercellular spaces in the inner cortex of lucerne nodules. Journal of Structural Biology 126, 59–71.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wesley-Smith J
(2001) Freeze-substitution of dehydrated plant tissues; artefacts of aqueous fixation revisited. Protoplasma 218, 154–167.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Williamson B, Duncan GH
(1989) Use of cryo-techniques with scanning electron microscopy to study infection of mature red raspberry fruits by Botrytis cinerea. New Phytologist 111, 81–88.
| Crossref | GoogleScholarGoogle Scholar |
Williamson RE,
Burn JE,
Birch R,
Baskin TI,
Betzner AS, Cork A
(2001) Morphology of rsw1, a cellulose-deficient mutant of Arabidopsis thaliana. Protoplasma 215, 116–127.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wirsel SGR,
Runge-Froböse C,
Ahrén DG,
Kemen E,
Oliver RP, Mendgen KW
(2002) Four or more species of Cladosporium sympatrically colonize Phragmites australis. Fungal Genetics and Biology 35, 99–113.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wu Y,
Machado AC,
White RG,
Llewellyn DJ, Dennis ES
(2006) Expression profiling identifies genes expressed early during lint fibre initiation in cotton. Plant & Cell Physiology 47, 107–127.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zoller S,
Frey B, Scheidegger C
(2000) Juvenile development and diaspore survival in the threatened epiphytic lichen species Sticta fuliginosa, Leptogium saturninum and Menegazzia terebrata: conclusions for in situ conservation. Plant Biology 2, 496–504.
| Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA, Holbrook NM
(2000) Bordered pit structure and vessel wall surface properties. Implications for embolism repair. Plant Physiology 123, 1015–1020.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
