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Supplemental Information

Chemical Priming Against Multiple Abiotic Stresses: Mission Possible?Andreas Savvides1,2, Shawkat Ali3, Mark Tester3, Vasileios Fotopoulos1

1Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of Technology, 3603 Lemesos, Cyprus.2Agrisearch Innovations Ltd, 2108 Nicosia, Cyprus. 3Center for Desert Agriculture, Division of Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, Thuwal 23955-6900, Saudi Arabia.Correspondence: [email protected] (V. Fotopoulos)

Table 1. The Effects Of Plant Pre-Treatment With The Chemical Agents Sodium Nitroprusside (SNP; NO Donor), Hydrogen Peroxide (H2O2), Sodium Hydrosulfide

(NaHS; H2S Donor), Melatonin, And Polyamines On The Molecular, Biochemical, Physiological, And Growth Traits Of Plants Subjected To Different Abiotic Stresses

Compared With Those Of Plants Without Pre-Treatment.

Priming

agent

Abiotic

stress

Plant

species

TissueMethod of

applicatio

n

Agent

treatment

duration/

interval

duration/Str

ess duration

Agent

concen-

tration

Molecular effects Biochemical effects

Physiological

and growth

effects

Summary/highlights Refs

Sodium Salinity Rice Treated: Nutrient 2d/0d/8d Tested: -↑Expression of stress-related -↑SOD, POX, CAT, APX, GR activities -↑surviving - Alleviation of the stress impacts is limited within S1

nitroprusside

(SNP)

Roots

Sampled:

Leaves

solution 0-1000μM

Optimum:

1μΜ

Toxic:

100 &

1000μM

genes (SPS, P5CS, HSP26) green parts (%),

PSII quantum

yield

a certain agent concentration range.

Citrus Treated:

Roots

Sampled:

Leaves

Incubation 2d/0d/16d Tested:

100μM

-↓DNA strand cleavage, protein

oxidation (carbonylation)

-↑SOD, CAT, APX, GR activities,

[ASC/DHA]a,

[GSH/GSSG], ∙OH scavenging activity

--- - Long-lasting systemic prime effect on the

antioxidant-related tolerance mechanism.

S2

Wheat Treated:

Seed

Sampled:

Germinating

seeds

Presoaking 20h/0d/5d Tested:

0.1mM

--- -↑ATP synthesis, [soluble sugars], [K+],

α-amylase activity, SOD & CAT activities,

-↓[seed starch], [Na+], [MDA], H2O2 &

O2•− release rate in mitochondria

-↑seed

respiration rate,

germination

rate, coleoptile

& radicle DW

-↓seed DW

- Alleviation of the impacts on seed germination,

seedling establishment & cell membrane integrity

- Enhanced antioxidant capacity & maintained

[Na+]/ [K+] balance.

S3

Wheat Treated:

Roots portion

Sampled:

Leaves

Incubation 1d/0d/4d Tested:

1mM

--- - ↑[AsA], [GSH], [GSH/GSSG], MDHAR,

DHAR, GR, GST, GPX, CAT, Gly I, Gly II

activities

- ↓[H2O2], [MDA]

-↓ Leaf

chlorosis/yellowi

ng

- Exogenous NO rendered the plants more

tolerant to salt-induced oxidative damage by

enhancing their antioxidant defense and MG

detoxification systems

S4

Citrus Treated:

Roots

Sampled:

Roots & leaves

Incubation 48h/0d/8d Tested:

100μM

- ↓ H2O2 and NO sources-related

transcripts after chemical agent

treatment in leaves & at the end

of the salt stress in roots, protein

carbonylation & nitration in leaves,

protein nitrosylation in roots

-↑ H2O2 and NO sources-related

transcripts at the end of the salt

stress in leaves, protein

nitrosylation in leaves

- ↑ local & systemic [H2O2] & [NO], [Chl],

- ↓ EL

- ↑

Photosynthetic

capacity

- No leaf

necrosis or

rolling

- H2O2 and NO generation are interlinked in

citrus, forming part of an active interplay

mechanism at the whole-plant level. This

mechanism involves spatio-temporal organization

and tissue-specific control at the transcriptional

level.

- ROS/RNS-mediated protein post-translational

modifications are a key molecular strategy for

signaling transduction and salinity acclimation.

S5

Strawberry Treated: Incubation Tested: Tested: - ↑Expression of genes associated - =[NO], [H2O2] -↑RWC, Ψw, - Alleviation of the stress impacts on leaf turgor, S6

Roots

Sampled:

Leaves

2d/0 or 7d/8d

Optimum:

2d/0d/8d

100μM with enzymatic antioxidants (cAPX,

CAT, GR, MnSOD, MDHAR, DHAR)

and ASC, GSH and RNS

biosynthesis

-↑[Chl], [Crt], [ASC/DHA],

[GSH/GSSG]

-↓EL, [MDA]

photosynthetic

electron

transport rate

-↓leaf wilting,

necrosis

photosynthesis and cell membrane integrity

- Redox regulation & antioxidant signaling are

key-targets of NO priming against salt stress

Drought Rice Treated:

Seed or leaves

Sampled:

leaves

Tested:

Presoaking

or foliar

spraying

Optimum:

F. spraying

2/---/21 seed

0/---/21 foliar

Tested:

0-150 μM

Optimum:

100 μM

--- - ↑[Free proline]

- ↓EL, [H2O2], [MDA]

- ↑

Photosynthetic

rate, RWC, Ψw,

Ψπ, Ψp,

seedling FW,

DW and height

- ↓ gs

- Maintenance of tissue water potential, enhanced

antioxidant system, improved stability of cellular

membranes, enhanced photosynthetic capacity

S7

Trifoliate

orange

Treated:

Shoot & roots

Sampled:

leaves

Spraying &

soil irrigation

14d/3d/7d Tested:

100 μM

--- -↑[NO], [Chl], SOD, POD, CAT activities

-↓ EL, [H2O2], [O2•−]

-↑

photosynthetic

rate

-↓ stomatal

aperture, gs

- Modulation of stomatal response, activation of

the antioxidant enzymes

S8

Heat Rice Treated:

Roots

Sampled:

Leaves

Nutrient

solution

Tested:

2d/0d/5h

Tested:

0-1000μM

Optimum:

1μΜ

-↑Expression of stress-related

genes (SPS, P5CS, HSP26)

-↑SOD, POX, CAT, APX, GR activities -↑surviving

green parts (%),

PSII quantum

yield

- Alleviation of the stress impacts is limited within


S1

Maize Treated:

---

Sampled:

Roots &

coleoptiles

--- 6h/0d/18h Tested:

0-400μM

Optimum:

150μM

Toxic:

≥200μM

--- -↑ L-DES activity, [H2S]

-↓EL, [MDA]

-↑Seedlings

survival

percentage,

tissue vitality

- Improved heat tolerance in a concentration-

dependent manner

- Crosstalk between NO and H2S in the

acquisition of heat stress tolerance

S9

Chilling Cucumber Treated:

Shoot

Sampled:

Leaves

Spraying 3d/0d/2d Tested:

0-2mM

Optimum:

1mM

--- - =[soluble protein]

-↑[Chl], [soluble sugars], SOD, POD, CAT,

GR activities

-↓[MDA]

-↓ Chilling

damage index

(chlorosis,

crinkled leaf

- Improved chilling tolerance by the activation of

antioxidant enzymes and osmotic adjustment

substances.

S10

Toxic:

2mM

edge, wilting,

dead leaves)

Wheat Treated:

Seed

Sampled:

Seeds & leaves

Presoaking 20h/0d/--- Tested:

0.1mM

- ↑ SOD encoding gene (Mn-SOD)

expression in seeds & seedlings

-↑α-amylase activity, SOD activity in

seeds & seedlings, [Chl], [soluble

sugars], [sucrose]

-↓[H2O2], [MDA], [starch]

-↑ Germination

rate, seed, seed

respiration rate,

seedling

establishment

and growth

- Improved cold tolerance by promoting β-

amylase activity hydrolysis of starch into

soluble sugars seed respiration & growth

& by enhancing the antioxidant system

S11

Tomato Treated:

Seed

Sampled:

Germinating

seeds &

seedlings

Presoaking 1d/0d/10d Tested:

200μΜ

--- -↑α-amylase, β-amylase activities,

[soluble sugars], seed [NO]

-↑ Germination

capacity, index,

seedling root

and shoot

length

- Improved cold tolerance at least partly by

promoting α- & β-amylase activity

S12

Excess

light

Tall Fescue Treated:

Root

Sampled:

Leaves

Nutrient

solution

---/---/7d Tested:

0-500μM

Optimum:

100μM

Toxic:

≥200μM

--- -↑SOD, CAT, APX, GR activities, NO

release

-↓EL, [MDA], [H2O2], [O2•−], LOX & NOS

activity

--- - Enhanced antioxidant enzymes activity &

reduced [ROS] & LOX activity prevented lipid

peroxidation and membrane damage

S13

Heavy

metals

(Cd)

Alfalfa Treated:

Roots

Sampled:

Roots

Nutrient

solution

6h/0h/12h Tested:

100μM

-↑Transcript levels of Cu/Zn-SOD

and POD

-↑SOD & POD activities, [NO] at the

onset of stress

-↓[TBARS], LOX activity, [Cd], [NO] at the

end of stress

-↑ Plant FW - Improved tolerance may be related with:

suppressed Cd uptake, enhanced antioxidant

system.

S14

Hydrogen

peroxide

Salinity Rice Treated:

Roots

Nutrient

solution

Tested:

2d/0d/8d

Tested:

0-1000μM




green parts (%),



S1

(H2O2) Sampled:

Leaves

Optimum:

10μΜ

PSII quantum

yield

Citrus Treated:

Roots

Sampled:

Leaves

Incubation Tested:

8h/0d/16d

Tested:

10mM

-↓DNA strand cleavage, protein

oxidation (carbonylation)

-↑SOD, CAT, APX, GR activities,

[ASC/DHA],

[GSH/GSSG], ∙OH scavenging activity

--- - Long-lasting systemic prime effect on the

antioxidant-related defense mechanism.

S2

Wheat Treated:

Seed

Sampled:

Leaves/ shoot

Presoaking 8h/0h/15d after

germination

Tested:

0-120μM

Optimum:

80μM

-↑Expression of heat-stable (stress)

proteins (32kDa, 52kDa)

- = shoot [Na+]

-↑shoot [K+], [K+]:[Na+], [Ca2+],

[NO3-], [PO43-]

-↓ shoot [H2O2], membrane

permeability, ion leakage

-↑ Germination

rate, shoot FW &

DW, leaf area,

net

photosynthesis,

gs, Ψw, Ψp

- H2O2-enhanced tolerance is linked to the

activation of antioxidants, maintaining turgor and

meeting plant nutritional requirement.

S15

Citrus Treated:

Roots

Sampled:

Roots & leaves

Incubation 8h/0d/8d Tested:

10mM

- ↓ H2O2 and NO sources-related

transcripts after chemical agent

treatment in leaves & at the end

of the salt stress in roots, protein

carbonylation & nitration in leaves,

protein nitrosylation in roots

-↑ H2O2 and NO sources-related

transcripts at the end of the salt

stress in leaves, protein

nitrosylation in leaves

- ↑ local & systemic [H2O2] & [NO], [Chl],

- ↓ EL

- ↑

Photosynthetic

capacity

- No leaf

necrosis or

rolling

- H2O2 and NO generation are interlinked in

citrus, forming part of an active interplay

mechanism at the whole-plant level. This

mechanism involves spatio-temporal organization

and tissue-specific control at the transcriptional

level.

- ROS/RNS-mediated protein post-translational

modifications are a key molecular strategy for

signaling transduction and salinity acclimation.

S5

Strawberry Treated:

Roots

Sampled:

Leaves

Incubation Tested:

8h/0 or 7d/8d

Optimum:

8h/0d/8d

Tested:

10mM

-↑Expression of genes associated

with enzymatic antioxidants (cAPX,

CAT, GR, MnSOD, MDHAR, DHAR)

and ASC, GSH and RNS

biosynthesis

- =[NO], [H2O2]

-↑[Chl], [Crt], [ASC/DHA],

[GSH/GSSG]

-↓EL, [MDA]

-↑RWC, Ψw,

photosynthetic

electron

transport rate

-↓leaf wilting,

necrosis

- Redox regulation & antioxidant signaling are

key-targets of H2O2 priming against salt stress

S6

Ginseng Treated:

Roots

Sampled:

Shoot & roots

Nutrient

solution

2d/0d/7d Tested:

0.05-250μM

Optimum:

100μM

-↑Expression of defense-related

genes (PGIP, ribonuclease-2 (PR-

10), chitinase (PR-2), calmodulin,

sesquiterpene synthase,

-↑APX, CAT, POX activities, [Chl], [Crt],

[Proline]

-↓[H2O2], [O2•−], [MDA]

-↑Plant height,

plant DW, RWC

- Alleviation of the stress impacts is related to

enhanced antioxidant system and osmotic

adjustment.

S16

Toxic:

>100μM

spermidine synthase)

Drought Wheat Treated:

Seed

Sampled:

Leaves/

Seedlings

Presoaking 6h/---/--- (exp.

ended when 3rd

leaf was fully

expanded)

Tested:

0-140mM

Optimum:

80mM

Toxic:

>80mM

--- -↑[Proline], CAT, APX activities

-↓[H2O2], [MDA]

-↑ Germination

rate, net

photosynthesis,

leaf area,

seedling DW,

WUE

- Alleviation of the stress impacts is related to

enhanced antioxidant system and osmotic

adjustment.

S17

Soybean Treated:

Shoot

Sampled:

Leaves

Spraying Sprayed

once/0d/8d

Tested:

1mM

-↑mRNA levels of GmMIPS2 & GolS

(encode key-enzymes for

oligosaccharides biosynthesis)

-↑[myo-inositol] & [galactinol] -↑ RWC, gs, net

photosynthesis,

-↓ Leaf wilting

- Enhanced tolerance due to the water content

maintenance caused by enhanced

oligosaccharides biosynthesis rather than by

rapid stomatal closure

S18

Heat Rice Treated:

Roots

Sampled:

Leaves

Nutrient

solution

2d/0d/5h Tested:

0-1000μM

Optimum:

10μΜ




green parts (%),

PSII quantum

yield


a certain agent concentration range

S1

Cucumber Treated:

Shoot

Sampled:

Leaves

Spraying Sprayed

once/12h/3d

Tested:

1.5mM

--- -↑GSH-Px, DHAR, MDHAR, GR, SOD, APX

-↓[H2O2], [MDA]

-↓abnormal

chloroplasts

- Protection of chloroplasts’ ultrastructure by the

enhanced antioxidant activity & decreased lipid

peroxidation

S19

Chilling Tomato Treated:

Roots

Sampled:

Leaves & roots

Incubation 1h/4d/16h Tested:

1mM

Optimum:

--- - = leaf APX, CAT activities, leaf [H2O2],

-↑leaf [anthocyanins], root [proline], root

APX, CAT activities

-↓root [H2O2], leaf & root [MDA]

-↑ RWC - Alleviation of the chilling stress maybe due to

enhanced antioxidant system and cellular

osmotic adjustment

S20

Excess

light

Tobacco Treated:

Shoot

Sampled:

Leaves

Spraying Sprayed

once/1d/1d

Tested:

0-500mM

Optimum:

5mM

--- -↑ CAT, APX & POX activities, GPX protein

levels, [GSH/GSSG]

-↓[MDA]

--- - Alleviation of the stress impacts is limited within

a certain agent concentration range

S21

Toxic:

500mM

Heavy

metals

(Cd)

Rice Treated:

---

Sampled:

Shoot & roots

--- 1d/0d/7d Tested:

100μΜ

--- - = Root [Cd], root APX, leaf GST, leaf

CAT activities, leaf [GSH], leaf & root

[GSSG], leaf & root [AsA], leaf [H2O2]

-↑ leaf & root SOD, root CAT, leaf & root

GPX, leaf APX, root GST activities, root

[GSH]

-↓ Shoot [Cd], Shoot [Cd] / Root [Cd],

root [H2O2], leaf & root [MDA]

-↑Shoot & root

length & DW

- The enhanced tolerance maybe due to a

stimulated antioxidant system and Cd

sequestration.

- The synthesis of GSH and GST were also

enhanced, which seems to regulate Cd

distribution in rice seedlings

S22

(Cr(VI)) Canola Treated:

Roots

Sampled:

Shoot & roots

Nutrient

solution

24h/0d/7d Tested:

200μM

-↑expression level of BnMP1 mRNA - = Root [Cr], SOD & CAT activities

-↑ Shoot [Cr], [Chl], POD & APX activities,

[Protein-bound & non-protein thiols]

-↓[MDA]

-↑Seedlings FW

& DW

- Thiol-containing chelators may play an

important role in the sequestration of Cr

S23

Sodium

hydrosulfide

(NaHS)

Salinity Strawberry Treated:

Roots

Sampled:

Leaves

Incubation Tested:

2d/0d/7d or

2d/3d/7d

Optimum:

2d/0d/7d

Tested:

100 μΜ

- Coordinated regulation of

multiple transcriptional

pathways

key antioxidant, ascorbate and

glutathione biosynthesis, RNS

biosynthesis, dehydration-

responsive element binding factor,

(DREB), and salt overly sensitive

(SOS) pathway genes.

- ↑[H2S], [ASC/DHA], [GSH/GSSG]

- ↓[MDA], [ROS], [RNS]

- ↑ RWC,

photosynthetic

capacity, gs, Ψw

- ↓ Wilting, foliar

injury

- Oxidative and nitrosative cellular damage

control through the increased performance of

antioxidative mechanisms and the coordinated

regulation of the SOS pathway

- Primed state is not long-lasting

S24

Drought Wheat Treated:

Roots

Sampled:

Leaves

Incubation 12h/0h/24h Tested:

0.5-2mM

Optimum:

1mM

Toxic:

≥1.5mM

--- - = MDHAR, GalLDH activity

- ↑[AsA], [GSH], [total ascorbate], [total

glutathione], APX, GR, DHAR, γ-ECS

activities

- ↓[MDA], EL

--- - H2S enhances the antioxidant ability

and protects wheat seedlings against oxidative

stress

induced by water stress

S25

Strawberry Treated:

Roots

Sampled:

Incubation Tested:

2d/0d/7d or

2d/3d/7d

Tested:

100 μΜ

Coordinated regulation of multiple

transcriptional pathwayskey

antioxidant, ascorbate and

-↑[H2S], [ASC/DHA], [GSH/GSSG]

-↓[MDA], [ROS], [RNS]

- ↑ RWC,

photosynthetic

capacity, gs, Ψw

- Oxidative and nitrosative cellular damage

control through the increased performance of

antioxidative mechanisms and the coordinated

S24

Leaves Optimum:

2d/0d/7d

glutathione biosynthesis, RNS

biosynthesis, dehydration-


(DREB), and salt overly sensitive

(SOS) pathway genes.

- ↓ Wilting, foliar

injury

regulation of the SOS pathway

- Primed states is not long-lasting

Heat Maize Treated:

---

Sampled:

Roots &

coleoptiles

--- 6h/0d/18h Tested:

0-1500μM

Optimum:

500μM

Toxic:

≥1000μM

--- -↑ L-DES activity, [H2S]

-↓EL, [MDA]

-↑Seedlings

survival

percentage,

tissue vitality

- H2S improves heat tolerance in a concentration-

dependent manner

S9

Strawberry Treated:

Roots

Sampled

Leaves


100μΜ

- Induction of gene expression

levels of enzymatic antioxidants

(cAPX, CAT, MnSOD, GR), heat

shock proteins (HSP70, HSP80,

HSP90), aquaporins (PIP)

- ↑[ASC], [GSH], [ASC/DHA], [GSH/GSSG]

- ↓ [H2S], [H2O2], [NO], [DHA], [GSSG],

[MDA]

- ↑

Photosynthetic

capacity

- ↓ Leaf wilting,

curling

- H2S root pretreatment activates a coordinated

network of heat shock defense-related pathways

at a transcriptional level and systemically

protects strawberry plants from heat

shock-induced damage.

S26

Chilling Grapevine Treated:

Leaves

Sampled

Leaves

Spraying 1h/0h/--- Tested:

0.1mM

-↑expression levels of VvICE1 &

VvCBF3

- ↑SOD activity

- ↓[O2•−], [MDA]

--- - H2S is involved in grapevine chilling stress

response by modulating VvICE1 and VvCBF3

transcription.

S27

Excess

light

Dendrobium

officinale

Treated:

Leaves

Sampled:

Leaves

Spraying Sprayed

once/0h/4h

Tested:

0- 600μM

Optimum:

200mM

Toxic:

≥400mM

--- - ↑ CAT, SOD, POD activities

- ↓ MDA content

- ↑

Photosynthetic

capacity

- ↓

Photoinhibition

- Enhanced tolerance against high light stress by

possibly increasing activities of antioxidant

enzymes and enhancing photosynthetic electron

transfer.

S28

Heavy

metals

(Al

toxicity)

Wheat Treated:

Seed

Sampled:

Seed


0-1.5mM

Optimum:

0.6mM

--- - ↑ amylase, esterase activities, APX,

CAT, POD, SOD activities, [H2S]

-↓[H2O2], [O2•−], [MDA], LOX activity,

[Al]

- ↑ Seed

germination %,

radicle &

coleoptile

length, radicle

-The H2S donor-induced lowering of H2O2 and

MDA levels could be attributed to the increased

activities of ROS scavenging enzymes and the

decreased activity of LOX.

S29

number

(Cd) Alfalfa Treated:

Roots

Sampled:

Roots

Nutrient

solution

6h/0h/12h Tested:

0-100μM

Optimum:

100μM

-↑Transcript levels of Cu/Zn-SOD

and POD

-↑SOD & POD activities, [NO] at the

onset of stress

-↓[TBARS], LOX activity, [Cd], [NO] at the

end of stress

-↑ Plant FW - Improved tolerance may be related with:

suppressed Cd uptake, enhanced antioxidant

system.

- NO might be a component of the H2S-induced

cytoprotective role

S14

(Cd) Populus

euphratica

Treated:

Cells

Sampled:

Cells

Medium 6h/0h/72h Tested:

0-200μM

Optimum:

50-100μM

--- -↑ APX, CAT, GR activities, vacuolar [Cd] /

cytoplasmic [Cd]

-↓ [H2O2], [MDA], Cd influx through

plasma membrane

- ↓ Programmed

cell death

- H2S attenuated Cd toxicity

by 1) up-regulating activity of antioxidant

enzymes, 2) reducing Cd entry into the

cytoplasm, and 3) increasing Cd sequestration

into the vacuole.

S30

Melatonin Salinity Malus Treated:

Roots

Sampled:

Leaves & roots

Nutrient

solution

10d/0d/15d Tested:

0.1μM

- ↑ transcripts of MDNHX1,

MdAKT1 in the leaves

- ↑ [Chl], dehydrogenase activity, APX,

CAT, POD activities, root & stem [Na+],

root & stem & leaves [K+], leaves

[K+]/[Na+]

- ↓ EL, [H2O2], leaves [Na+]

- ↑ Plant height,

leaf number,

plant FW & DW,

net

photosynthesis,

- Melatonin is involved in the activation of

antioxidants & the modulation of ion

homeostasis as shown by the up-regulation of the

ion transporters in leaves

S31

Soybean Treated:

Seeds

Sampled:

Seeds & leaves

Coating ---/7d/22d Tested:

0-200 μM

Optimum:

50-100μM

-↑Many stress-responsive genes

e..g. ferredoxin gene (PetF),

ascorbate metabolism-related

genes (VTC4, APX4).

- ↑ [Chl]

- ↓ EL, [H2O2]

- ↑ Biomass,

shoot height,

leaf area

- Melatonin up-regulates many salt-inhibited

genes and may increase salt tolerance partly via

antioxidant capacity enhancement

S32

Bermudagras

s

Treated:

Roots

Sampled:

Leaves

Irrigation 7d/0d/25d Tested:

0- 100 μΜ

Optimum:

20, 100 μM

- ↑ Many stress-responsive genes:

e.g. CBF/DREB genes and target

genes, heat shock TFs, zing finger

TFs, WRKY, MYB, bHLH genes and

hormone-related genes

- ↑ [Melatonin], [Chl] SOD, CAT, POD

activities, GSH redox state, [metabolites]

e.g. amino acids, sugars, sugar alcohols

- ↓ [H2O2], [O2•−], EL, [MDA]

- ↑Survival rate,

plant height,

plant weight

- Melatonin is involved in the activation of

antioxidants, modulation of metabolic

homeostasis & extensive transcriptional

reprogramming.

S33

Drought Bermudagras

s

Treated:

Root

Sampled:

Irrigation 7d/0d/21d/4d

recovery

Tested:

0- 100 μΜ

Optimum:

Same as salt stress Same as salt stress Same as salt

stress

Same as salt stressS33

Leaves 20, 100 μM

Malus Treated:

Roots

Sampled:

Leaves

Nutrient

solution

10d/0d/6d Tested:

100 μΜ

-↓ Expression of melatonin

synthesis genes, ABA biosynthesis

genes, ABA catabolism genes

- ↑CAT, POD, APX enzymes activity, [Chl],

[Crt]

- ↓EL, [H2O2], [ABA]

- ↑ RWC, net

photosynthesis,

gs, stomatal

size and

aperture

- Melatonin enhances ABA degradation and

suppresses its synthesis and thus less H2O2

accumulates in guard cells, directly scavenges

H2O2, up-regulates the antioxidant system

S34

Heat Phacelia

tanacetifolia

Treated:

Seed

Sampled:

Germinating

seeds

Presoaking 2d/2h/7d Tested:

0-90μΜ

Optimum:

0.3-6μΜ

--- --- - ↑ germination

percentage &

rate,

- Melatonin enhances heat stress toleranceS35

Chilling Wheat Treated:

Shoot

Sampled:

Leaves

Spraying 12h/0d/3d Tested:

0,1mM

- ↑Rubisco expression - ↑[Chl], [Crt], [Proline], [soluble protein],

[Phenolic compounds], carbohydrate

accumulation, SOD, GPX, APX, GR

activities, [AsA], [GSH]

- ↓ [DHA], DHA/AsA, GSSG/GSH, [H2O2],

[O2•−], [MDA]

- ↑ RWC, leaf

area

- Melatonin directly scavenges H2O2, enhances

the antioxidant system and photosynthesis and

increase the cellular accumulation of

osmoprotectants.

S36

Arabidopsis Treated:

Roots

Sampled:

Seedlings

Culture

medium

Tested:

1d/0d/3d or

1d/0d/5d

Tested:

0 - 400 μM

Optimum:

10 - 40 μM

Toxic:

>100μM

- ↑ expression of:

C-repeat-binding factors (CBFs),

Drought Response Element

Binding factors (DREBs), a cold-

responsive gene, COR15a, a

transcription factor involved in

freezing and drought-stress

tolerance CAMTA1 and

transcription activators of reactive

oxygen species (ROS)-related

antioxidant genes, ZAT10 and

ZAT12

--- - ↑ FW, primary

root length, and

shoot height

- Melatonin induces

cold signaling genes up-regulation resulting in

cold-protecting compounds biosynthesis

S37

Freezing Bermudagras Treated: Irrigation 7/0/21cold/ Same as salt stress Same as salt stress Same as salt Same as salt stressS33

s Roots

Sampled:

Leaves

8freezing stress

Heavy

metal

(Cu

toxicity)

Red cabbage Treated:

Seed

Sampled:

Germinating

seeds &

seedlings

Hydropriming ---/3d/5d seed

exp.

---/3d/8d

seedling exp.

Tested:

1-100 μM

Optimum:

1-10 μM

Deleterious

:

100 μM

- ↓ DNA endoreduplication blocking - ↓ Lipid peroxidation ([TBARS]) - ↑ Seed

germination

percentage and

rate, seedling

FW

- Melatonin may enhance tolerance to Cu partly

by enhancing the antioxidant system

S38

Polyamines

(Spermidine)

Salinity Rice

(tolerant-

sensitive)

Treated:

Shoot

Sampled:

Grains

Spraying 7d/0d/--- Tested:

1mM

--- - ↓[Na+]/[K+] - ↑ Grain yield

(62% sensitive,

16% tolerant)

- Spermidine largely enhanced yield.

- Spermidine enhanced ion homeostasis.

S39

(Spermidine) Rice Treated:

Seed

Sampled:

Leaves

Presoaking 12h/17d/10d Tested:

1mM

--- - ↑ [Phenolic compounds], [Chl],

[anthocyanins], antioxidant capacity

- ↓[H2O2], [Na+]/[K+]

- ↑ shoot FW,

DW, length

- Long-lasting priming phenomenon

- Spermidine enhances salt tolerance by

increasing antioxidant capacity and ion

homeostasis

S40

(Spermidine) Salinity

&

alkalinity

Tomato Treated:

Seed

Sampled:

Roots

Presoaking 10h/-/6d Tested:

0.25mM

--- - = [free Putrescine]

- ↑ [Free spermidine], [free spermine]

- ↑ Root DW - Exogenous Spd can regulate the metabolic

status of polyamines

S41

(Spermine) Drought Citrus Treated:

Roots

Sampled:

Leaves

Incubation 5d/12h/12h Tested:

1mM

- ↑ Expression levels of ADC &

SPMS (polyamines biosynthesis)

- ↑ [Polyamines], SOD, POD activities

- ↓ EL, [H2O2], [O2•−]

- ↓ Water loss,

stomatal

aperture

- Spm pretreatment causes enhanced

endogenous polyamines, effective ROS

scavenging, and stimulated stomatal closure

S42

(Spermine) Soybean Treated:

Shoot

Sampled:

Pods

Spraying 3d/14d/--- Tested:

0.1mM

Optimum:

--- - = [GSH]

- ↑SOD, CAT activities, [polyphenols],

[Protein]

- ↓ [ABA], [MDA]

- ↑ Pods & seeds

FW,

- Long-lasting tolerance enhancement

- Increased yield

S43

(Spermidine) White clover Treated: Presoaking 3h/0d/7d Tested: - = Transcript level of α-amylase - ↑ α-amylase, β-amylase activities, seed

[reducing sugars], [fructose], [glucose],

- ↑ germination

%, vigor, index,

-The discrepancy between gene expression and

enzyme activity indicates enzyme activity

S44

Seed

Sampled:

Seed &

seedlings

30μM - ↑ Transcript level of β-amylase,

relative expression ratio of Cu/Zn

SOD, CAT, POD, APX

SOD, CAT, POD, APX activities, [AsA],

[AsA]/[DHA], [GSH], [GSH]/[GSSG]

- ↓ seed [starch], [MDA], EL, [H2O2],

[O2•−], [DHA]

rate root

viability, length,

seedling FW,

DW

changes were

not only caused by mRNA levels, but also

regulated at the post-transcriptional level and

influenced by

cellular metabolism

- the function of Spd is

double 1) a stress-protecting compound and 2)

signaling molecule

(Putrescine) Flooding Onion Treated:

Roots

Sampled:

Leaves

Soil

drenching

24h/0d/10d Tested:

0-3mM

Optimum:

2mM

--- - ↑ [Chl], scavenging activity, metal

chelating capacity

- ↓ [H2O2], [O2•−],

- ↑ RWC, plant

height,

photosynthetic

capacity

- Putrescine protective

action against flooding may be related to its iron

binding capacity & enhancement of antioxidant

system

S45

(Spermine, T-

spermine,

spermidine,

putrescine)

Heat Arabidopsis Treated:

Roots

Sampled:

Seedlings

Incubation ---/0h/2h Tested:

0-1mM

Optimum:

0.1mM

Toxic:

≥0.5mM

--- - ↑ [Chl] - ↑ vigorously

growing leaves

& roots

- ↓ cotyledons

chlorosis

- Spermine alleviated heat stress (HS) effects

best

- Spermine increases the HS response at

transcriptional

and translational levels (from research on

transgenic & mutant plants)

S46

(Spermidine) Rice Treated:

Shoot

Sampled:

Leaves

Spraying 24h/0h/48h/

recovery 48h

Tested:

0-2mM

Optimum:

1mM

--- - ↑ [Chl], [AsA], [GSH], AsA & GSH redox

status, SOD, CAT, GPX, GST, APX, DHAR,

GR, GLY I, GLY II activities, [free

spermidine], [soluble conjugated

spermidine]

- ↓ [MDA], [H2O2], [proline], LOX activity

- ↑ leaf FW - Enhancement of the antioxidative and

glyoxalase systems by spermidine rendered rice

seedlings more tolerant to heat stress

S47

(Spermine) Heat &

Drought

Trifoliate

orange

Treated:

Roots

Sampled:

Leaves


1mM

- ↑ expression of heat shock

proteins, abscisic acid (ABA)-


9-cic-epoxycarotenoid

dioxygenase 3

- ↑ SOD, POD, CAT activities

- ↓ EL, [H2O2], [O2•−],

- ↓ leaf wilting,

water loss

- Polyamines may confer tolerance to multiple

simultaneously applied stresses

S48

(Putrescine,

spermidine)

Chilling Cucumber Treated:

Shoot

Sampled:

Spraying Sprayed

once/12h/3d/

recovery 1d

Tested:

0.5mM

--- - ↑ endogenous [polyamines], [soluble

proteins], SOD, POD, CAT, APX activities

- ↓ EL, [MDA], [H2O2]

--- - Enhanced cold tolerance may be partly related

to enhanced antioxidant capacity and

osmoprotectants

S49

Leaves

(Putrescine,

spermidine,

spermine, 1,3-

diaminopropan

e,

diethylenetriam

ine)

Freezing Wheat Treated:

Shoot

Sampled:

Leaves

Spraying Sprayed

once/24h /24h

Tested:

100mg/l

--- - ↑ [Chl] , [Proline]

- ↓ EL

- ↑ shoot FW,

survival rate

- Polyamines are capable of preventing frost

injuries

- Diethylenetriamine was the most effective

S50

(Spermine)

Heavy

metals

(Cd)

Wheat Treated:

Leaf segments

Sampled:

Leaf segments


1mM

--- - = [GSH], APX activity

- ↑ [spermidine], [spermine], GR activity

- ↓ [TBARS], [H2O2]

--- - Spermine enhances Cd stress toleranceS51

(Spermine) (Cu) Wheat Treated:

Leaf segments

Sampled:

Leaf segments


1mM

--- - = [GSH], APX activity

- ↑[Putrescine], [spermidine], [spermine],

GR activity

- ↓ [TBARS] , [H2O2]

--- - Spermine enhances Cu stress tolerance partly

by enhancing antioxidant capacity

S51

Abbreviations: ABA: abscisic acid, APX: ascorbate peroxidase, AsA: ascorbic acid, ASC: reduced ascorbate, ASC/DHA: ascorbate redox state, CAT: catalase, Chl: chlorophyll, Crt: Carotenoids, DAO: diamine oxidase, DHA: dehydroascorbate, DHAR: dehydroascorbate reductase, DW: dry weight, EL: electrolyte leakage, FW: fresh weight, GalLDH: L-Galactono-1,4-lactone dehydrogenase, gs: stomatal conductance, GPX: glutathione peroxidase, GR: glutathione reductase, GSH: reduced glutathione, GSH/GSSG: glutathione redox state, GSH-Px: glutathione peroxidase, GSSG: oxidized glutathione, Gly I: glyoxalase I, Gly II: glyoxalase II, GST: glutathione S-transferase, L-DES: L-cystine desulfhydrase, LOX: lipoxygenase, MDA: malondialdehyde, MDHAR: monodehydrascorbate reductase, MG: methylglyoxal, NOS: nitric oxide synthase, ODC, ornithine decarboxylase, PAO: polyamine oxidase, POD: peroxidase, POX: guaiacol peroxidase, RLW: leaf relative water content, RNS: reactive nitrogen species, ROS: reactive oxygen species, SAMDC: S-adenosylmethionine decarboxylase, SOD: superoxide dismutase, TBARS: thiobarbituric acid reactive substances, WUE: water use efficiency, γ-ECS: gamma-glutamylcysteine synthetase, Ψp: pressure potential, Ψw: leaf water potential, Ψπ: osmotic potentiala[ ]: concentration, ↑: increase, ↓: decrease, =: not altered,

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