Paper · 2019 · PeerJ

Metabolic alterations in pea leaves during arbuscular mycorrhiza development

Oksana Y. Shtark; Roman K. Puzanskiy; Galina S. Avdeeva; et al.

13
claims
26
verbatim quotes
38
citations
3
research areas
✓
Open access · cc-by

Abstract

Arbuscular mycorrhiza (AM) is known to be a mutually beneficial plant-fungal symbiosis; however, the effect of mycorrhization is heavily dependent on multiple biotic and abiotic factors. Therefore, for the proper employment of such plant-fungal symbiotic systems in agriculture, a detailed understanding of the molecular basis of the plant developmental response to mycorrhization is needed. The aim of this work was to uncover the physiological and metabolic alterations in pea ( Pisum sativum L.) leaves associated with mycorrhization at key plant developmental stages. Plants of pea cv. Finale were grown in constant environmental conditions under phosphate deficiency. The plants were analyzed at six distinct time points, which corresponded to certain developmental stages of the pea: I: 7 days post inoculation (DPI) when the second leaf is fully unfolded with one pair of leaflets and a simple tendril; II: 21 DPI at first leaf with two pairs of leaflets and a complex tendril; III: 32 DPI when the floral bud is enclosed; IV: 42 DPI at the first open flower; V: 56 DPI when the pod is filled with green seeds; and VI: 90–110 DPI at the dry harvest stage. Inoculation with Rhizophagus irregularis had no effect on the fresh or dry shoot weight, the leaf photochemical activity, accumulation of chlorophyll a , b or carotenoids. However, at stage III (corresponding to the most active phase of mycorrhiza development), the number of internodes between cotyledons and the youngest completely developed leaf was lower in the inoculated plants than in those without inoculation. Moreover, inoculation extended the vegetation period of the host plants, and resulted in increase of the average dry weight per seed at stage VI. The leaf metabolome, as analyzed with GC-MS, included about three hundred distinct metabolites and showed a strong correlation with plant age, and, to a lesser extent, was influenced by mycorrhization. Metabolic shifts influenced the levels of sugars, amino acids and other intermediates of nitrogen and phosphorus metabolism. The use of unsupervised dimension reduction methods showed that (i) at stage II, the metabolite spectra of inoculated plants were similar to those of the control, and (ii) at stages IV and V, the leaf metabolic profiles of inoculated plants shifted towards the profiles of the control plants at earlier developmental stages. At stage IV the inoculated plants exhibited a higher level of metabolism of nitrogen, organic acids, and lipophilic compounds in comparison to control plants. Thus, mycorrhization led to the retardation of plant development, which was also associated with higher seed biomass accumulation in plants with an extended vegetation period. The symbiotic crosstalk between host plant and AM fungi leads to alterations in several biochemical pathways the details of which need to be elucidated in further studies.

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Claims 13

Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Inoculation with Rhizophagus irregularis had no effect on fresh or dry shoot weight or on leaf photochemical activity in pea.

Material
Finalee0
Treatment
Inoculation with Rhizophagus irregularise1
Interactor
Rhizophagus irregularisRhizophagus irregularise1symbiont
Outcome
fresh or dry shoot weight, the leaf photochemical activitye1
Direction
no effecte1

Not reportedComparator

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗
Rhizophagus irregularis
Rhizophagus irregularis · InteractorMylène Durant · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“Inoculation with Rhizophagus irregularis had no effect on the fresh or dry shoot weight, the leaf photochemical activity, accumulation of chlorophyll a , b or carotenoids”

✓ located verbatim in the source · abstract, characters 1163–1333 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Inoculation with Rhizophagus irregularis had no effect on accumulation of chlorophyll a, chlorophyll b or carotenoids in pea.

Material
Finalee0
Treatment
Inoculation with Rhizophagus irregularise1
Interactor
Rhizophagus irregularisRhizophagus irregularise1symbiont
Outcome
accumulation of chlorophyll a , b or carotenoidse1
Direction
no effecte1

Not reportedComparator

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗
Rhizophagus irregularis
Rhizophagus irregularis · InteractorMylène Durant · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“Inoculation with Rhizophagus irregularis had no effect on the fresh or dry shoot weight, the leaf photochemical activity, accumulation of chlorophyll a , b or carotenoids”

✓ located verbatim in the source · abstract, characters 1163–1333 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

At stage III, inoculated pea plants had fewer internodes between cotyledons and the youngest completely developed leaf than plants without inoculation.

Organ / stage
stage IIIe1
Treatment
inoculatede1
Outcome
number of internodes between cotyledons and the youngest completely developed leafe1
Direction
lowere1
Comparator
those without inoculatione1

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“at stage III (corresponding to the most active phase of mycorrhiza development), the number of internodes between cotyledons and the youngest completely developed leaf was lower in the inoculated plants than in those without inoculation”

✓ located verbatim in the source · abstract, characters 1344–1580 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Inoculation extended the vegetation period of the pea host plants.

Treatment
inoculatione1
Outcome
vegetation periode1
Direction
extendede1

Not reportedComparator

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“Moreover, inoculation extended the vegetation period of the host plants, and resulted in increase of the average dry weight per seed at stage VI”

✓ located verbatim in the source · abstract, characters 1582–1726 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Inoculation increased the average dry weight per seed at stage VI in pea.

Organ / stage
stage VIe1
Treatment
inoculatione1
Outcome
average dry weight per seede1
Direction
increasee1

Not reportedComparator

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“Moreover, inoculation extended the vegetation period of the host plants, and resulted in increase of the average dry weight per seed at stage VI”

✓ located verbatim in the source · abstract, characters 1582–1726 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

The pea leaf metabolome analysed by GC-MS included about three hundred distinct metabolites.

Outcome
leaf metabolomee1
Value
about three hundred distinct metabolitese1

Not reportedDirection

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“The leaf metabolome, as analyzed with GC-MS, included about three hundred distinct metabolites and showed a strong correlation with plant age”

✓ located verbatim in the source · abstract, characters 1728–1869 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

The pea leaf metabolome showed a strong correlation with plant age.

Organ / stage
plant agee1
Outcome
leaf metabolomee1

Not reportedDirection

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“The leaf metabolome, as analyzed with GC-MS, included about three hundred distinct metabolites and showed a strong correlation with plant age”

✓ located verbatim in the source · abstract, characters 1728–1869 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

The pea leaf metabolome was influenced by mycorrhization to a lesser extent than by plant age.

Treatment
mycorrhizatione1
Outcome
influencede1
Qualifier
to a lesser extente1

Not reportedComparatorDirection

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“showed a strong correlation with plant age, and, to a lesser extent, was influenced by mycorrhization”

✓ located verbatim in the source · abstract, characters 1827–1928 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Metabolic shifts influenced the levels of sugars, amino acids and other intermediates of nitrogen and phosphorus metabolism in pea leaves.

Outcome
levels of sugars, amino acids and other intermediates of nitrogen and phosphorus metabolisme1

Not reportedDirection

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“Metabolic shifts influenced the levels of sugars, amino acids and other intermediates of nitrogen and phosphorus metabolism”

✓ located verbatim in the source · abstract, characters 1930–2053 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

At stage II, leaf metabolite spectra of inoculated pea plants were similar to those of the control.

Organ / stage
stage IIe1
Treatment
inoculatede1
Outcome
metabolite spectrae1
Direction
similare1
Comparator
the controle1

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“at stage II, the metabolite spectra of inoculated plants were similar to those of the control”

✓ located verbatim in the source · abstract, characters 2123–2216 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

At stages IV and V, leaf metabolic profiles of inoculated pea plants shifted towards the profiles of control plants at earlier developmental stages.

Organ / stage
stages IV and Ve1
Treatment
inoculatede1
Outcome
leaf metabolic profilese1
Direction
shifted towardse1
Comparator
control plantse1

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“at stages IV and V, the leaf metabolic profiles of inoculated plants shifted towards the profiles of the control plants at earlier developmental stages”

✓ located verbatim in the source · abstract, characters 2227–2378 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

At stage IV, inoculated pea plants had higher metabolism of nitrogen, organic acids and lipophilic compounds than control plants.

Organ / stage
stage IVe1
Treatment
inoculated plantse1
Outcome
level of metabolism of nitrogen, organic acids, and lipophilic compoundse1
Direction
highere1
Comparator
control plantse1

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“At stage IV the inoculated plants exhibited a higher level of metabolism of nitrogen, organic acids, and lipophilic compounds in comparison to control plants”

✓ located verbatim in the source · abstract, characters 2380–2537 · show in text ↑
Intervention effectauthor interpretationoriginal resultmeasured

Claim · model-written summary

The authors conclude that mycorrhization led to retardation of pea plant development.

Treatment
mycorrhizatione1
Outcome
plant developmente1
Direction
retardatione1

Not reportedComparator

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

Lathyrus oleraceus
Lathyrus oleraceus · TaxonRenee Comet (photographer) AV Number: AV-9400-4164 · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Plants of pea cv. Finale”

✓ located verbatim in the source · abstract, characters 572–596 · show in text ↑
e1

“mycorrhization led to the retardation of plant development”

✓ located verbatim in the source · abstract, characters 2545–2603 · show in text ↑

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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.