Paper · 2019 · Frontiers in Plant Science

Flooding Responses on Grapevine: A Physiological, Transcriptional, and Metabolic Perspective

Benedetto Ruperti; Alessandro Botton; Francesca Populin; et al.

10
claims
17
verbatim quotes
74
citations
3
research areas
✓
Open access · cc-by

Abstract

Studies on model plants have shown that temporary soil flooding exposes roots to a significant hypoxic stress resulting in metabolic re-programming, accumulation of toxic metabolites and hormonal imbalance. To date, physiological and transcriptional responses to flooding in grapevine are poorly characterized. To fill this gap, we aimed to gain insights into the transcriptional and metabolic changes induced by flooding on grapevine roots (K5BB rootstocks), on which cv Sauvignon blanc (Vitis vinifera L.) plants were grafted. A preliminary experiment under hydroponic conditions enabled the identification of transiently and steadily regulated hypoxia-responsive marker genes and drafting a model for response to oxygen deprivation in grapevine roots. Afterwards, over two consecutive vegetative seasons, flooding was imposed to potted vines during the late dormancy period, to mimick the most frequent waterlogging events occurring in the field. Untargeted transcriptomic and metabolic profiling approaches were applied to investigate early responses of grapevine roots during exposure to hypoxia and subsequent recovery after stress removal. The initial hypoxic response was marked by a significant increase of the hypoxia-inducible metabolites ethanol, GABA, succinic acid and alanine which remained high also one week after recovery from flooding with the exception of ethanol that levelled off. Transcriptomic data supported the metabolic changes by indicating a substantial rearrangement of primary metabolic pathways through enhancement of the glycolytic and fermentative enzymes and of a subset of enzymes involved in the TCA cycle. GO and KEGG pathway analyses of differentially expressed genes showed a general down-regulation of brassinosteroid, auxin and gibberellin biosynthesis in waterlogged plants, suggesting a general inhibition of root growth and lateral expansion. During recovery, transcriptional activation of gibberellin biosynthetic genes and down-regulation of the metabolic ones may support a role for gibberellins in signaling grapevine rootstocks waterlogging metabolic and hormonal changes to the above ground plant. The significant internode elongation measured upon budbreak during recovery in plants that had experienced flooding supported this hypothesis. Overall integration of these data enabled us to draft a first comprehensive view of the molecular and metabolic pathways involved in grapevine’s root responses highlighting a deep metabolic and transcriptomic reprogramming during and after exposure to waterlogging.

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Claims 10

Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Flooding significantly increased ethanol, GABA and succinic acid in grapevine roots during the hypoxic response.

Taxon
grapevineVitise0
Treatment
floodinge0
Outcome
ethanol, GABA, succinic acide1
Direction
increasee1

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e1

“The initial hypoxic response was marked by a significant increase of the hypoxia-inducible metabolites ethanol, GABA, succinic acid and alanine”

✓ located verbatim in the source · abstract, characters 1147–1290 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Flooding significantly increased alanine in grapevine roots during the hypoxic response.

Taxon
grapevineVitise0
Treatment
floodinge0
Outcome
alaninee1
Direction
increasee1

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e1

“The initial hypoxic response was marked by a significant increase of the hypoxia-inducible metabolites ethanol, GABA, succinic acid and alanine”

✓ located verbatim in the source · abstract, characters 1147–1290 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Hypoxia-inducible metabolites remained high one week after recovery, except ethanol, which levelled off.

Taxon
grapevineVitise0
Outcome
remained high also one week after recoverye2
Qualifier
with the exception of ethanol that levelled offe2

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e2

“which remained high also one week after recovery from flooding with the exception of ethanol that levelled off”

✓ located verbatim in the source · abstract, characters 1291–1401 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Flooding rearranged primary metabolic pathways in grapevine roots through enhanced glycolytic and fermentative enzymes.

Taxon
grapevineVitise0
Organ / stage
rootse0
Outcome
rearrangement of primary metabolic pathwayse3
Qualifier
through enhancement of the glycolytic and fermentative enzymese3

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e3

“indicating a substantial rearrangement of primary metabolic pathways through enhancement of the glycolytic and fermentative enzymes”

✓ located verbatim in the source · abstract, characters 1458–1589 · show in text ↑
Associationobservedoriginal resultnegativemeasured

Claim · model-written summary

Waterlogged grapevine plants showed general down-regulation of brassinosteroid, auxin and gibberellin biosynthesis.

Taxon
grapevineVitise0
Treatment
waterlogged plantse4
Outcome
brassinosteroid, auxin and gibberellin biosynthesise4
Direction
down-regulatione4

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e4

“GO and KEGG pathway analyses of differentially expressed genes showed a general down-regulation of brassinosteroid, auxin and gibberellin biosynthesis in waterlogged plants, suggesting a general inhibition of root growth and lateral expansion”

✓ located verbatim in the source · abstract, characters 1644–1886 · show in text ↑
Associationhypothesisoriginal resultnegativemeasured

Claim · model-written summary

Waterlogging may generally inhibit root growth and lateral expansion of grapevine.

Taxon
grapevineVitise0
Treatment
waterlogged plantse4
Outcome
root growth and lateral expansione4
Direction
inhibitione4

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e4

“GO and KEGG pathway analyses of differentially expressed genes showed a general down-regulation of brassinosteroid, auxin and gibberellin biosynthesis in waterlogged plants, suggesting a general inhibition of root growth and lateral expansion”

✓ located verbatim in the source · abstract, characters 1644–1886 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

During recovery, gibberellin biosynthetic genes were transcriptionally activated in grapevine rootstocks.

Taxon
grapevineVitise5
Gene
gibberellin biosynthetic genese5
Outcome
transcriptional activation of gibberellin biosynthetic genese5
Qualifier
During recoverye5

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e5

“During recovery, transcriptional activation of gibberellin biosynthetic genes and down-regulation of the metabolic ones may support a role for gibberellins in signaling grapevine rootstocks waterlogging metabolic and hormonal changes to the above ground plant”

✓ located verbatim in the source · abstract, characters 1888–2147 · show in text ↑
Mechanismhypothesisoriginal resultbasis n/a

Claim · model-written summary

Gibberellins may signal waterlogging-induced metabolic and hormonal changes from grapevine rootstocks to the aerial plant.

Taxon
grapevineVitise5
Compound
gibberellinse5
Outcome
metabolic and hormonal changese5

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e5

“During recovery, transcriptional activation of gibberellin biosynthetic genes and down-regulation of the metabolic ones may support a role for gibberellins in signaling grapevine rootstocks waterlogging metabolic and hormonal changes to the above ground plant”

✓ located verbatim in the source · abstract, characters 1888–2147 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

During recovery, metabolic gibberellin biosynthetic genes were down-regulated in grapevine rootstocks.

Taxon
grapevineVitise5
Outcome
down-regulation of the metabolic onese5

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e5

“During recovery, transcriptional activation of gibberellin biosynthetic genes and down-regulation of the metabolic ones may support a role for gibberellins in signaling grapevine rootstocks waterlogging metabolic and hormonal changes to the above ground plant”

✓ located verbatim in the source · abstract, characters 1888–2147 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

Flooding during dormancy significantly increased internode elongation upon budbreak during recovery in grapevine.

Taxon
grapevineVitise0
Treatment
floodinge6
Outcome
internode elongatione6
Direction
increaseinferrede6
Qualifier
upon budbreak during recoverye6

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Vitis
Vitis · Taxon · picture of the genus (one of its species)Victor M. Vicente Selvas · Public domain · Wikimedia Commons ↗

Verbatim

e0

“flooding on grapevine roots (K5BB rootstocks)”

✓ located verbatim in the source · abstract, characters 413–458 · show in text ↑
e6

“The significant internode elongation measured upon budbreak during recovery in plants that had experienced flooding”

✓ located verbatim in the source · abstract, characters 2149–2264 · show in text ↑

flooding · molecular: metabolites · VitisPositive and negative results

2 papers: 1 positive, 1 negative or no effect

1 in the opposite direction

  1. negative
See all 2 papers →

flooding · growth · VitisPositive and negative results

4 papers: 2 positive, 2 negative or no effect

1 paper in the same direction as this paper · 2 in the opposite direction

  1. negative
  2. negative
  3. positive
See all 4 papers →

Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.