Role of Pit Membranes in Macromolecule-Induced Wilt of Plants

Alfen, Neal K. Van; McMillan, Brent D.; Turner, Victoria; Hess, W. M.

doi:10.1104/pp.73.4.1020

Cited by 38 publications

(21 citation statements)

References 7 publications

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“…There is a strong implication from these studies that pores in the range capable of permitting air seeding exist in most of the inter-vessel pit membranes. For example, experiments which estimate pore size from reduction of hydraulic conductance by dextrans or spheres (Van Alfen et al, 1983;Jarbeau et al, 1995) require that the majority of membranes contain pores that are close to the defined range of particle sizes.…”

Section: Discussionmentioning

confidence: 99%

“…These include microscopic observation of Sphagnum spp. halocysts (Lewis, 1988), comparison of air injection and water stress-induced vulnerability curves (Cochard et al, 1992;Sperry and Saliendra, 1994), and reduction of hydraulic conductance by dextrans (Van Alfen et al, 1983) or latex nanospheres (Jarbeau et al, 1995). There is a strong implication from these studies that pores in the range capable of permitting air seeding exist in most of the inter-vessel pit membranes.…”

Section: Discussionmentioning

confidence: 99%

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Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species

et al. 2003

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Aspects of xylem anatomy and vulnerability to water stress-induced embolism were examined in stems of two droughtdeciduous species, Brachychiton australis (Schott and Endl.) A. Terracc. and Cochlospermum gillivraei Benth., and two evergreen species, Alphitonia excelsa (Fenzal) Benth. and Austromyrtus bidwillii (Benth.) Burret., growing in a seasonally dry rainforest. The deciduous species were more vulnerable to water stress-induced xylem embolism. B. australis and C. gillivraei reached a 50% loss of hydraulic conductivity at Ϫ3.17 MPa and Ϫ1.44 MPa, respectively; a 50% loss of hydraulic conductivity occurred at Ϫ5.56 MPa in A. excelsa and Ϫ5.12 MPa in A. bidwillii. To determine whether pit membrane porosity was responsible for greater vulnerability to embolism (air seeding hypothesis), pit membrane structure was examined. Expected pore sizes were calculated from vulnerability curves; however, the predicted inter-specific variation in pore sizes was not detected using scanning electron microscopy (pores were not visible to a resolution of 20 nm). Suspensions of colloidal gold particles were then perfused through branch sections. These experiments indicated that pit membrane pores were between 5 and 20 nm in diameter in all four species. The results may be explained by three possibilities: (a) the pores of the expected size range were not present, (b) larger pores, within the size range to cause air seeding, were present but were rare enough to avoid detection, or (c) pore sizes in the expected range only develop while the membrane is under mechanical stress (during air seeding) due to stretching/flexing.Xylem cavitation and embolism are recognized as major constraints affecting plants regularly exposed to water stress (Tyree and Sperry, 1989;Milburn, 1993). Water in the xylem is under negative pressure, or tension, i.e. it is held in a metastable state, below its vapor pressure, a condition that increases the likelihood of cavitation occurring (Oertli, 1971;Pickard, 1981). Cavitation is the process whereby a vapor phase is introduced to the xylem water column, creating an embolism. Embolisms are gas bubbles consisting initially of water vapor and later air, which become trapped within xylem conduits. Because of its inability to transmit tension, the vapor phase limits the volume flow of water through the conduit, reducing the plant's capacity to deliver water to the canopy (Meinzer et al., 2001). Plants must minimize this disruption to water transport to avoid effects on leaf water status that may result in limitations on stomatal conductance and photosynthesis.The structure of xylem vessels is seen as an important factor in determining the occurrence of water stress-induced cavitation (Zimmermann, 1983). Xylem vessels are bounded by pit membranes, through which water must pass to move from one vessel to the next. Pit membranes are the degraded primary cell walls and middle lamella of the vessels and are composed of tightly inter-woven cellulose microfibrils in a matrix of hemicellulose and pectin polysaccharide...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species

et al. 2003

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“…Dimond, 1966;Eiscus, Parsons & Albertc, 1973;Zimmcrmann, 1978;Tyree et al,, 1983;Ewers, 1985), pathogen modes of action (e.g. Dimond, 1970;Suhayda & Goodman, 1981;Van Alfen et aL, 1983;Newbanks, Bosch & Zimmermann, 1983), and methods of wood preservation (e.g. Anderson, Gortncr & Schmitz, 1941).…”

Section: Introductionmentioning

confidence: 99%

A method for measuring hydraulic conductivity and embolism in xylem

Sperry

Donnelly

Tyree

1988

Plant Cell & Environment

973

788

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Abstract. Hydraulic conductivity of the xylem is computed as the quotient of mass fiow rate and pressure gradient. Measurements on excised plant stems can be difficult to interpret because of timedependent reductions in fiow rate, and because of variable degrees of embolism. Using Acer saccharum Marsh, stems, we found that certain perfusing solutions including dilute fixatives (e.g. 0.05% formaldehyde) and acids with pH below 3 (e.g. 10 mol m~^ oxalic) prevent long-term decline in conductivity. Xylem embolism can be quantified by expressing the initial conductivity as a percentage of the maximum obtained after fiow-impeding air emboli have been removed by repeated high-pressure (175 kPa) fiushes. Correlation between microbial contatnination and declining conductivity suggests that long-tenn (>4h) declines are caused by microbial growth within the vessels. Unpredictable trends in short-term (<4h) measurements may be caused by movements of air emboli in vessels and/or particulate matter.

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“…This was first suggested by Hussain and Kelman (19), who observed that EPS-containing culture supernatants could wilt tomato cuttings and that spontaneous mutants lacking EPS were nonvirulent. The mechanism of wilt induction may involve occlusion of xylem pit membranes (34). However, EPS may also contribute to virulence by other means.…”

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confidence: 99%

Genetic and biochemical characterization of a Pseudomonas solanacearum gene cluster required for extracellular polysaccharide production and for virulence

Cook

1991

J Bacteriol

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Infection of host plants by Pseudomonas solanacearum results in wilting, which is thought to be due largely to the occlusion of xylem vessels by the P. solanacearum extracellular polysaccharide (EPS) that primarily consists of N-acetylK gld me (GaINAc). By means of Ta3 mutagenesis, we identified a 6.5-kb gene cluster that contains five complementation units required for EPS production and virulence in this bacterium. There was positive correlation between the amount of EPS produced in culture and (i) in planta growth and (ii)virulence. Based on analysis of 0-glucuronidase-gene fusions, these genes are expressed both in broth cultures and in planta and may be constitutive. Both wild-type and mutant strains contained similar amounts of UDP-GaINAc, the predicted primary substrate for EPS synthesis. Thus, the EPS mutants we obtained should be useful in the analysis of steps in the assembly of the polysaccharide and how this process is related to virulence.Virulence in Pseudomonas solanacearum (E.F.Sm.) is a complex and multifaceted phenomenon. Most of the known or presumed virulence factors in P. solanacearum are extracellular products, including the plant cell wall-degrading enzymes polygalacturonase (3, 27) and endoglucanase (26) and the plant hormones auxin, cytokinin, and ethylene (9). Although this array of extracellular products would seem to constitute a formidable arsenal for virulence, the most intensively studied virulence factor from P. solanacearum is a relatively inert product, extracellular polysaccharide (EPS) (1,11,13,19,31,36,38). This high-molecular-weight polymer is thought to be responsible for induction of the wilt symptoms that characterize the disease caused by P. solanacearum.Wild-type virulent strains of P. solanacearum produce EPS that forms a loosely associated slime both in culture and in planta. Since the pathogen is limited primarily to plant xylem vessels, EPS is thought to cause wilt symptoms by obstructing water flow. This was first suggested by Hussain and Kelman (19) (1, 11, 13), but the presence of these sugars is probably the result of incomplete purification. Instead, two amino sugars, bacillosamine (2,4-diamino-2,4,6-trideoxyglucose) and galactosaminuronic acid, probably are integral components of the P. solanacearum EPS. The latter sugar is apparently responsible for the acidic nature of the molecule (33a).Most of the early work on the relationship of EPS to virulence in P. solanacearum was based on spontaneous EPS-mutants. However, interpretation of results obtained with these mutants is confounded by the fact that such mutants are pleiotropic and are affected in other characteristics that also are likely to be important for virulence (9,25

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Role of Pit Membranes in Macromolecule-Induced Wilt of Plants

Cited by 38 publications

References 7 publications

Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species

Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species

A method for measuring hydraulic conductivity and embolism in xylem

Genetic and biochemical characterization of a Pseudomonas solanacearum gene cluster required for extracellular polysaccharide production and for virulence

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