Mycorrhizal Fungi Enhance Host Crop Mycorrhizal Fungi Enhance Host Crop Resistance to Abiotic StressResistance to Abiotic Stress
Fred DaviesFred Davies
Dept. Horticultural SciencesDept. Horticultural SciencesTexas A&M UniversityTexas A&M UniversityCollege Station, TexasCollege Station, Texas
Texas Lignite Coal Industry Texas Lignite Coal Industry
Drag LineDrag Line Coal SeamCoal Seam
Disturbed SiteDisturbed SiteNonNon--AMAM +AM+AM
Vesicular Arbuscular MycorrhizaVesicular Arbuscular Mycorrhiza
Arbuscular Mycorrhizal Enhancement of Plant Water RelationsArbuscular Mycorrhizal Enhancement of Plant Water Relations
AMF enhancement of drought resistance may be response to better AMF enhancement of drought resistance may be response to better host nutritionhost nutrition——particularly particularly
PhosphorusPhosphorus (Safir & Nelson, 1985);(Safir & Nelson, 1985); Nitrogen Nitrogen (Subramanian, 2003)(Subramanian, 2003)
AMF affect mechanisms that control plant water relations such aAMF affect mechanisms that control plant water relations such as:s:
Leaf gas exchangeLeaf gas exchange (Hardie 1985; Davies et al. 1993; Koide 1993)(Hardie 1985; Davies et al. 1993; Koide 1993)
Generally higher stomatal conductance and transpirationGenerally higher stomatal conductance and transpiration ((Augé 2001)Augé 2001)
Turgor maintenanceTurgor maintenance-- osmotic adjustmentosmotic adjustment (Aug(Augéé et al 1986)et al 1986)
PhytohormonePhytohormone production production (Duan et al 1995, Nikolaou et al. 2003, Estrada(Duan et al 1995, Nikolaou et al. 2003, Estrada--Luna & Luna & Davies, 2003)Davies, 2003)
Nonhydraulic root to shoot communication of soil dryingNonhydraulic root to shoot communication of soil drying (Augé & Dunn 1991)(Augé & Dunn 1991)
Root hydraulic conductivityRoot hydraulic conductivity (Sweatt & Davies 1984; Nelson 1987; Cui & Nobel 1992;(Sweatt & Davies 1984; Nelson 1987; Cui & Nobel 1992;Syvertsen & Graham 1990)Syvertsen & Graham 1990)
AMF Enhancement of Plant Water Relations (con.)AMF Enhancement of Plant Water Relations (con.)
••Extraradical hyphae developmentExtraradical hyphae development--improved root/soil contact (30 to 100 m /g soil)improved root/soil contact (30 to 100 m /g soil)
(Benthlenfalvay et al, 1988, Davies et al, 1992)(Benthlenfalvay et al, 1988, Davies et al, 1992)
••Enhancement of soil structure, aggregate stability and subsequenEnhancement of soil structure, aggregate stability and subsequent available soil watert available soil water(Aug(Augéé et al. 2001)et al. 2001)
••Greater carbon allocation (sinkGreater carbon allocation (sink--regulated) to rootsregulated) to roots (Wright et al. 1998)(Wright et al. 1998)
Morphological ChangesMorphological Changes
Higher rootHigher root--shoot ratio, greater lateral root formation, leaf abscissionshoot ratio, greater lateral root formation, leaf abscission (Henderson & (Henderson & Davies, 1990); Davies, 1990);
Leaf expansionLeaf expansion (Koide, 1985)(Koide, 1985)
Better droughtBetter drought--acclimated AMF plants (greater plant fitness).acclimated AMF plants (greater plant fitness).
Drought can enhance colonization & extraradical hyphae formationDrought can enhance colonization & extraradical hyphae formation of AMF.of AMF.
Plant Water RelationsPlant Water Relations
•• Plant Acclimation to DroughtPlant Acclimation to Drought
••Acclimatization of TC produced plantletsAcclimatization of TC produced plantlets
Drought Resistance [Levitt, 1980;Augé 2001](low external H2O potential)
Dehydration Tolerance Dehydration Avoidance
(Survival at low internal H2O content) (Maintain high internal H2O content)
Drought Tolerance(Survival at low internal H2O potential)
Drought AvoidanceDrought Avoidance(Maintain high internal H2O pot.)
APPROACH :APPROACH :
Compare AMF and NonCompare AMF and Non--AMF plants of comparable size AMF plants of comparable size and tissue nutritional status.and tissue nutritional status.
Acclimate plants to droughtAcclimate plants to drought via repetitive drought via repetitive drought cyclescycles (bell pepper, (bell pepper, Rosa hybridaRosa hybrida), or a slowly ), or a slowly developing drought cycle (chile ancho peppers, developing drought cycle (chile ancho peppers, neem tree seedlings). neem tree seedlings).
Capsicum annuum
(Bell peppers)
Glomus deserticola
Bell PepperBell Pepper: Capsicum annuum: Capsicum annuum L. ‘Early Bountiful’L. ‘Early Bountiful’
AMF: AMF: Glomus deserticolaGlomus deserticola
Fertilization: LANS 22 Fertilization: LANS 22 µµg P mlg P ml--11 AMF; NonAMF 44 AMF; NonAMF 44 µµg P mlg P ml--11
Drought AcclimatedDrought Acclimated (DA) (DA) ––Predawn Predawn ΨΨleafleaf --0.9 MPa; 0.9 MPa; ΨΨsoilsoil --0.5 MPa0.5 MPaNondrought AcclimatedNondrought Acclimated (Non(Non--DA) DA) ––Predawn Predawn ΨΨleaf leaf --0.2 MPa;0.2 MPa;
1/2 plants subjected to four DA cycles1/2 plants subjected to four DA cyclesDA and Nondrought acclimated plants subjected to droughtDA and Nondrought acclimated plants subjected to droughtDA and NDA given a 3DA and NDA given a 3--day recovery cycle.day recovery cycle.
Leaf water potential (Leaf water potential (ΨΨleafleaf ) of bell pepper ) of bell pepper during peak drought & recoveryduring peak drought & recovery
Leaf osmotic potential (Leaf osmotic potential (ΨΨππ) of bell pepper ) of bell pepper during peak drought & recoveryduring peak drought & recovery
Net photosynthesis (A) of bell pepper Net photosynthesis (A) of bell pepper during peak drought & recoveryduring peak drought & recovery
AMF Enhancement of Drought StressAMF Enhancement of Drought Stress--Bell PepperBell Pepper
AMF Peppers have:AMF Peppers have:Leaf ChlorophyllLeaf Chlorophyll
Stomatal ConductanceStomatal Conductance
PhotosynthesisPhotosynthesis
Osmotic AdjustmentOsmotic Adjustment
Faster Drought RecoveryFaster Drought Recovery
Phosphorus & plant size Phosphorus & plant size not not the limiting factorthe limiting factor
AMF Pepper Plants have:AMF Pepper Plants have:••Greater Extraradical Hyphae formationGreater Extraradical Hyphae formation
••Greater Soil AggregationGreater Soil Aggregation
•Improved Soil Tilth
•Glomalin – hydrophobic protein
→→ Not all mycorrhiza respond equally to droughtNot all mycorrhiza respond equally to drought
Chile ancho pepper: Chile ancho pepper:
••Glomus fasciculatumGlomus fasciculatum (Trappe, Oregon) (Trappe, Oregon)
••ZACZAC--1919: : mixed mixed Glomus Glomus species: species: G. albidiumG. albidium, , G. claroidesG. claroides, , G. diaphamumG. diaphamum
(Zacatecas, Mexico; 450 mm annual Precipitation; (Zacatecas, Mexico; 450 mm annual Precipitation; Chamizo, FerreraChamizo, Ferrera--Cerrato, 1998)Cerrato, 1998)
AMF Drought Soil Moist.(%)
ψleaf
(-Mpa)
gs
(mmol m-2
s-1)
RWC
(%)
Whole Plant Transpiration(mg H2O
m-2 s-1)
WUE(10-3. g. kg-1)
∆(‰)
Control No 17.0±1.4 0.1±0 268±14 92.6±1.4 48.2±1.4 5.34 18.9G. fasc. 18.3±0.4 0.1±0 257±13 88.9±1.1 48.1±1.4 5.29 18.7
ZAC-19 18.8±0.2 0.1±0 233±19 93.0±1.9 46.7±2.1 5.09 18.8
Control Yes 3.9±0.1 0.7±0.1 57±7 80.2±3.4 30.1±1.7 5.55 19.1G. fasc. 3.8±0.1 0.8±0.1 46±4 79.3±1.0 27.1±1.6 5.68 19.2
ZAC-19. 4.1± 0.4 0.2±0 51±4 84.4±1.9 25.4±1.9 5.58 19.2
SignificanceAMF NS 0.0001 NS NS NS NS NSDrought (D) 0.0001 0.0001 0.0001 0.0001 0.0001 NS NSAMF X (D) NS 0.0001 NS NS NS NS NS
Chile Ancho pepper plants during peak drought stress (day 20).Chile Ancho pepper plants during peak drought stress (day 20).
AMF Drought % Plantsnot wilted
% Plants moderatelywilted
% Plantsseverely wilted
Control Yes 0±0 47±12. 53±12
G. fasc. 0±0 26±10 74±10ZAC-19. 0±0 79±10 21±11
SignificanceAMF NS 0.0026 0.0089Drought (D) 0.0001 0.0001 0.0001AMF x D NS 0.0026 0.0089
Wilting of Chile Ancho pepper plants Wilting of Chile Ancho pepper plants ---- peak drought stress (day 20).peak drought stress (day 20).
Effect of Drought Stress on Colonization of Chile Ancho pepperEffect of Drought Stress on Colonization of Chile Ancho pepper
Control Glomus Glomus fasciculatumfasciculatum ZacZac--1919
DroughtDrought
NoNo 00 56.4a56.4a 37.5b
YesYes 00 21.6b21.6b 43.0a
(Pr>F)(Pr>F) NSNS 0.00010.0001 NSNS
DroughtDrought
NoNo 00 81.4a81.4a 29.9
YesYes 00 42.8b42.8b 26.1
(Pr>F)(Pr>F) NSNS 0.00010.0001 NSNS
DroughtDrought
NoNo 00 90.2a90.2a 51.9b
YesYes 00 62.7b62.7b 59.9a
(Pr>F)(Pr>F) NSNS 0.00010.0001 0.0030.003
% Arbuscule Formation
% Vesicle Formation
% Total Root Colonization
Neem (Azadirachta indica)
Glomus intraradicies
Vesicles
Appressorium
Table 2.Table 2. Growth parameters of mycorrhizal (AMF) and NonGrowth parameters of mycorrhizal (AMF) and Non--VAM VAM neem plants at the end of the drought stress cycle neem plants at the end of the drought stress cycle (23 days of drought followed (23 days of drought followed by a 1 day recovery).by a 1 day recovery).
AMF AMF DroughtDroughtacclimationacclimation
LeafLeafNo.No.
Leaf Leaf areaarea
Plant dry mass (g)Plant dry mass (g) Root/Root/shootshootratioratio
(m(m22))LeafLeaf(g) (g)
StemStem(g)(g)
RootRoot(g)(g) (g.g(g.g--11))
NonAMFNonAMF
AMFAMF
SignificanceSignificanceAMFAMFDroughtDroughtAMF x DAMF x D
NoNoYesYesNoNoYesYes
2929±±222121±±222929±±222323±±22
NSNS****NSNS
0.200.20±±0.010.010.140.14±±0.010.010.200.20±±0.010.010.140.14±±0.010.01
NSNS****
NSNS
1818±±111111±±111818±±111212±±11
NSNS****
NSNS
1111±±1188±±11
1111±±0099±±11
NSNS****
NSNS
1111±±1199±±00
1212±±1199±±00
NSNS****
NSNS
0.380.38±±0.030.030.470.47±±0.030.030.400.40±±0.020.020.430.43±±0.030.03
NSNS****
NSNS
AMF Effects on Neem Tree SeedlingsAMF Effects on Neem Tree Seedlings
±± AMF neem trees of similar size and nutrition respond to drought AMF neem trees of similar size and nutrition respond to drought similarly.similarly.
Neem drought response: decrease in leaf area, gas exchange rate Neem drought response: decrease in leaf area, gas exchange rate and water and water relations parameters. relations parameters.
Rapid recovery after rehydration with an acclimation of stomatalRapid recovery after rehydration with an acclimation of stomatal conductance.conductance.
Water Use EfficiencyWater Use Efficiency
Dry Mass gain per total water usage Dry Mass gain per total water usage ––(g Carbon/kg H(g Carbon/kg H22O) O) [Long Term][Long Term]
Gas Exchange: net Photosynthesis/ stomatal Gas Exchange: net Photosynthesis/ stomatal conductance conductance ((AA) / () / (ggss) ) [Instantaneous][Instantaneous]
Table 1. Wager Use Efficiency (WUE) in leaves of wellTable 1. Wager Use Efficiency (WUE) in leaves of well--watered and drought watered and drought stressed AMF and Nonstressed AMF and Non--AMF neem plants during 23 days of drought followed AMF neem plants during 23 days of drought followed by a 1 day recovery (day 24).by a 1 day recovery (day 24).
MycorrhizaMycorrhiza Drought Drought stressstress
Water Use EfficiencyWater Use Efficiency
(g DM/ kg H(g DM/ kg H22O)O)(AMF)(AMF)
NoninoculatedNoninoculated
InoculatedInoculated
SignificanceSignificanceAMFAMFDroughtDroughtInteractionInteraction
NoNoYesYesNoNoYesYes
2.52.50.90.92.42.41.21.2
NSNS****
NSNS
Water Use EfficiencyWater Use Efficiency (con)(con)
Stable Isotope Discrimination Stable Isotope Discrimination (C(C1313/C/C1212))
WUE not greater in AMF plantsWUE not greater in AMF plants
Table 1. Carbon isotope discrimination (Table 1. Carbon isotope discrimination (∆∆) in leaves of well) in leaves of well--watered and watered and drought stressed AMF and Nondrought stressed AMF and Non--AMF neem plants during 23 days of AMF neem plants during 23 days of drought followed by a 1 day recovery (day 24).drought followed by a 1 day recovery (day 24).
MycorrhizaMycorrhiza Drought Drought stressstress
∆∆ ((‰‰))
(AMF)(AMF) Day 0Day 0 Day 24Day 24Mature leavesMature leaves Expanding leavesExpanding leaves Mature leavesMature leaves
NoninoculatedNoninoculated
InoculatedInoculated
SignificanceSignificanceAMFAMFDroughtDroughtInteractionInteraction
NoNoYesYesNoNoYesYes
20.7120.71±±0.170.1720.5420.54±±0.420.4220.3220.32±±0.260.2620.3020.30±±0.370.37
NSNSNSNSNSNS
21.6721.67±±0.260.2618.6618.66±±0.230.2321.4721.47±±0.120.1219.0319.03±±0.590.59
NSNS****
NSNS
20.8120.81±±0.240.2420.3520.35±±0.510.5121.2221.22±±0.280.2820.1820.18±±0.350.35
NSNSNSNSNSNS
Inoculation TechniqueInoculation Technique
Spore Slurry Solution:Spore Slurry Solution:
AMF BandingAMF Banding
AMF --MICROPROPAGATED CHILE ANCHO PEPPER PLANTLETS DURING ACCLIMATIZATION AND POST-ACCLIMATIZATION
Growth Chamber 5 daysDay 1 — Near 100 % RHDay 2 — Near 100 %Day 3 — 80 %Day 4 — 70 %Day 5 — 60 %ExplantExplant
Rooted ExplantRooted Explant 55--Day Growth ChamberDay Growth Chamber
Day 6: Transfer to GHDay 6: Transfer to GH
TransplantTransplant
Transplantation of Chile Ancho
Development of mycorrhiza in micropropagated chile ancho pepper Development of mycorrhiza in micropropagated chile ancho pepper ((Capsicum annuumCapsicum annuum L. cv. San Luis) plantlets during acclimatization L. cv. San Luis) plantlets during acclimatization
and postand post--acclimatization acclimatization ((EstradaEstrada--Luna & Davies, 2003).Luna & Davies, 2003).
Noncolonized (NonAMF) Noncolonized (NonAMF) and AMF micropropagated and AMF micropropagated chile ancho pepper chile ancho pepper ((Capsicum annuumCapsicum annuum L. cv. L. cv. San Luis) plantlets during San Luis) plantlets during acclimatization and postacclimatization and post--acclimatization acclimatization ((EstradaEstrada--Luna & Davies, 2003).Luna & Davies, 2003).
Relative water Relative water content [RWC]content [RWC]
Transpiration [Transpiration [EE]]
Stomatal conductanceStomatal conductance
Photosynthesis [Photosynthesis [AA]]
Leaf chlorophyll of noncolonized (NonAMF) and AMF micropropagateLeaf chlorophyll of noncolonized (NonAMF) and AMF micropropagated d chile ancho pepper (chile ancho pepper (Capsicum annuumCapsicum annuum L. cv. San Luis) plantlets during L. cv. San Luis) plantlets during acclimatization and postacclimatization and post--acclimatization. acclimatization. ((EstradaEstrada--Luna & Davies, 2003).Luna & Davies, 2003).
Abscisic acid (ABA) in Abscisic acid (ABA) in noncolonized (NonAMF) noncolonized (NonAMF) and AMF micropropagated and AMF micropropagated chile ancho pepper chile ancho pepper ((Capsicum annuumCapsicum annuum L. cv. L. cv. San Luis) plantlets during San Luis) plantlets during acclimatization acclimatization ((EstradaEstrada--Luna & Davies, 2003).Luna & Davies, 2003).
Leaf ABALeaf ABA
Stem ABAStem ABA
Root ABARoot ABA
SummarySummaryAMF can enhance plant water relations independent of tissue P.AMF can enhance plant water relations independent of tissue P.
Differences among AMF isolates in plant water relations.Differences among AMF isolates in plant water relations.
AMF not more Water Use EfficientAMF not more Water Use Efficient
Decreased ABA.Decreased ABA.
Drought stress can enhance AMF symbiosis.Drought stress can enhance AMF symbiosis.
AMF plants are better acclimated to drought (greater plant fitnAMF plants are better acclimated to drought (greater plant fitness)ess)
Importance of Extraradical HyphaeImportance of Extraradical Hyphae--associated soil characteristicsassociated soil characteristics--soil moisture retentionsoil moisture retention
Mechanistic understanding of AMF & Water relations is incompleMechanistic understanding of AMF & Water relations is incomplete te (Safir et. al, 1972; Reid, 1979; Aug(Safir et. al, 1972; Reid, 1979; Augéé 2001, 2003)2001, 2003)
CollaboratorsCollaboratorsL. AguileraL. Aguilera--GomezGomez
M.J. AlvaradoM.J. Alvarado
A. AlarconA. Alarcon
M. A. ArnoldM. A. Arnold
S.H. BoS.H. Bo
T.W. BouttonT.W. Boutton
C. CalderónC. Calderón
C.A. CallC.A. Call
L. Amaya de CarpioL. Amaya de Carpio
A.A. CartmillCartmill
S.E. NewmanS.E. Newman
R.J. NewtonR.J. Newton
L. PhavuphutanonL. Phavuphutanon
J.R. PotterJ.R. Potter
V. OlaldeV. Olalde--PortugalPortugal
J.D. Puryear J.D. Puryear
J.A. Saraiva GrossiJ.A. Saraiva Grossi
M.E. StrongM.E. Strong
S.E. SvensonS.E. Svenson
M.E. SweattM.E. Sweatt
M.C. DrewM.C. Drew
S.A. DurayS.A. Duray
J.N. EgillaJ.N. Egilla
A. EstradaA. Estrada--LunaLuna
R.C. FerreraR.C. Ferrera--CerratoCerrato
YY--C HeC He
J.C. HendersonJ.C. Henderson--ColeCole
Z. Huaman Z. Huaman
R.G. Linderman R.G. Linderman
J.C. Miller, Jr.J.C. Miller, Jr.
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