Paper · 2024 · International Journal of Molecular Sciences

Root-Knot Nematode Early Infection Suppresses Immune Response and Elicits the Antioxidant System in Tomato

Sergio Molinari; Anna Carla Farano; Paola Leonetti

10
claims
22
verbatim quotes
9
citations
3
research areas
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Open access · cc-by

Abstract

The immune response in plants is regulated by several phytohormones and involves the overexpression of defense genes, including the pathogenesis-related (PR-) genes. The data reported in this paper indicate that nematodes can suppress the immune response by inhibiting the expression of defense genes. Transcripts from nine defense genes were detected by qRT-PCR in the roots of tomato plants at three and seven days post-inoculation (dpi) with living juveniles (J2s) of Meloidogyne incognita (root-knot nematodes, RKNs). All the salicylic acid (SA)-responsive genes tested (PR-1, PR-2, PR-4b, PR-5) were down-regulated in response to nematode infection. On the contrary, the expression of jasmonic acid (JA)-responsive genes, including ACO (encoding the enzyme 1-aminocyclopropane-1-carboxylic acid oxidase, which catalyzes the last step of ethylene (ET) biosynthesis) and JERF3 (Jasmonate Ethylene Response Factor 3), was unaffected by the infection. Conversely, the effect of nematode attack on the activities of the defense enzymes endoglucanase and endochitinase, encoded by PR-2 and PR-3, respectively, changed depending on the tested dpi. At 5 dpi, both enzymes were inhibited in inoculated plants compared to healthy controls. The genes encoding glutathione peroxidase (GPX) and catalase (CAT), both part of the antioxidant plant system, were highly overexpressed. Additionally, the activity of the antioxidant enzymes superoxide dismutase (SOD), CAT, and ascorbate peroxidase (APX) was enhanced in infected roots. Isoelectrofocusing of root extracts revealed novel SOD isoforms in samples from inoculated plants. Furthermore, plants were pre-treated with an array of key compounds, including hormone generators, inhibitors of SA or JA-mediated defense pathways, reactive oxygen species (ROS) scavengers and generators, inhibitors of ROS generation, and compounds that interfere with calcium-mediated metabolism. After treatments, plants were inoculated with RKNs, and nematodes were allowed to complete their life cycle. Factors of plant growth and infection level in treated plants were compared with those from untreated inoculated plants. Generally, compounds that decreased SA and/or ROS levels increased infection severity, while those that reduced JA/ET levels did not affect infection rates. ROS generators induced resistance against the pests. Compounds that silence calcium signaling by preventing its intake augmented infection symptoms. The data shown in this paper indicate that SA-mediated plant immune responses are consistently suppressed during the early stages of nematode infection, and this restriction is associated with the activation of the antioxidant ROS-scavenging system.

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Claims 10

Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Nematode infection down-regulated all tested salicylic-acid-responsive PR genes in tomato roots.

Treatment
nematode infectione0
Interactor
Meloidogyne incognitaMeloidogyne incognitae1pathogen
Gene
PR-1, PR-2, PR-4b, PR-5e0
Outcome
salicylic acid (SA)-responsive genese0
Direction
down-regulatede0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Meloidogyne incognita
Meloidogyne incognita · InteractorPhoto by William Wergin and Richard Sayre. Colorized by Stephen Ausmus. U.S. Department of Agriculture · CC BY 2.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“All the salicylic acid (SA)-responsive genes tested (PR-1, PR-2, PR-4b, PR-5) were down-regulated in response to nematode infection.”

✓ located verbatim in the source · abstract, characters 522–654 · show in text ↑
e1

“Meloidogyne incognita (root-knot nematodes, RKNs)”

✓ located verbatim in the source · abstract, characters 471–520 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Nematode infection left tomato ACO and JERF3 gene expression unaffected.

Treatment
infectione0
Gene
ACOe0
Outcome
expression of jasmonic acid (JA)-responsive genese0
Direction
unaffectede0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“the expression of jasmonic acid (JA)-responsive genes, including ACO (encoding the enzyme 1-aminocyclopropane-1-carboxylic acid oxidase, which catalyzes the last step of ethylene (ET) biosynthesis) and JERF3 (Jasmonate Ethylene Response Factor 3), was unaffected by the infection.”

✓ located verbatim in the source · abstract, characters 672–952 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

At five days after inoculation, nematodes inhibited tomato root endoglucanase and endochitinase activities relative to healthy controls.

Organ / stage
5 dpie0
Treatment
inoculated plantse0
Outcome
activities of the defense enzymes endoglucanase and endochitinasee1
Direction
inhibitede0
Comparator
healthy controlse0

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“At 5 dpi, both enzymes were inhibited in inoculated plants compared to healthy controls.”

✓ located verbatim in the source · abstract, characters 1146–1234 · show in text ↑
e1

“activities of the defense enzymes endoglucanase and endochitinase”

✓ located verbatim in the source · abstract, characters 1002–1067 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Antioxidant GPX and CAT genes were highly overexpressed in infected tomato roots.

Gene
GPXe0
Outcome
genes encoding glutathione peroxidase (GPX) and catalase (CAT)e0
Direction
highly overexpressede0

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“The genes encoding glutathione peroxidase (GPX) and catalase (CAT), both part of the antioxidant plant system, were highly overexpressed.”

✓ located verbatim in the source · abstract, characters 1235–1372 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Antioxidant SOD, CAT and APX activities were enhanced in infected tomato roots.

Organ / stage
infected rootse0
Outcome
activity of the antioxidant enzymes superoxide dismutase (SOD), CAT, and ascorbate peroxidase (APX)e0
Direction
enhancede0

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“the activity of the antioxidant enzymes superoxide dismutase (SOD), CAT, and ascorbate peroxidase (APX) was enhanced in infected roots.”

✓ located verbatim in the source · abstract, characters 1387–1522 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Inoculated tomato roots showed novel SOD isoforms.

Organ / stage
root extractse0
Gene
SODe0
Outcome
novel SOD isoformse0

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“Isoelectrofocusing of root extracts revealed novel SOD isoforms in samples from inoculated plants.”

✓ located verbatim in the source · abstract, characters 1523–1621 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Treatments that decreased salicylic acid or ROS increased nematode infection severity in tomato.

Treatment
compounds that decreased SA and/or ROS levelse0
Outcome
infection severitye0
Direction
increasede0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“compounds that decreased SA and/or ROS levels increased infection severity”

✓ located verbatim in the source · abstract, characters 2162–2236 · show in text ↑
Intervention effectobservedoriginal resultno effectmeasured

Claim · model-written summary

Treatments that reduced JA or ET did not affect nematode infection rates in tomato.

Treatment
those that reduced JA/ET levelse0
Outcome
infection ratese0
Direction
did not affecte0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“those that reduced JA/ET levels did not affect infection rates.”

✓ located verbatim in the source · abstract, characters 2244–2307 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

ROS generators induced tomato resistance to root-knot nematodes.

Treatment
ROS generatorse0
Outcome
resistance against the pestse0

Not reportedComparatorDirection

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“ROS generators induced resistance against the pests.”

✓ located verbatim in the source · abstract, characters 2308–2360 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

Compounds that silence calcium signaling increased nematode infection symptoms in tomato.

Treatment
Compounds that silence calcium signaling by preventing its intakee0
Outcome
infection symptomse0
Direction
augmentede0

Not reportedComparator

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

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

t0

“Tomato”

✓ located verbatim in the source · title, characters 100–106 · show in text ↑
e0

“Compounds that silence calcium signaling by preventing its intake augmented infection symptoms.”

✓ located verbatim in the source · abstract, characters 2361–2456 · show in text ↑

calcium atom · disease · Solanum lycopersicum (tomato)Results differ

50 papers: 35 positive, 15 negative or no effect

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  1. positive
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ethene · disease · Solanum lycopersicum (tomato)Positive and negative results

9 papers: 5 positive, 4 negative or no effect

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jasmonic acid · disease · Solanum lycopersicum (tomato)Positive and negative results

9 papers: 4 positive, 5 negative or no effect

4 papers in the same direction as this paper · 4 in the opposite direction

  1. positive
  2. positive
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salicylic acid · disease · Solanum lycopersicum (tomato)Positive and negative results

39 papers: 35 positive, 4 negative or no effect

3 papers in the same direction as this paper · 35 in the opposite direction

  1. positive
  2. positive
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infection · Meloidogyne incognita · Solanum lycopersicum (tomato)Positive and negative results

19 papers: 9 positive, 10 negative or no effect

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infection · molecular: expression · Solanum lycopersicum (tomato)Positive and negative results

38 papers: 26 positive, 12 negative or no effect

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inoculation · physiology: antioxidant enzymes · Solanum lycopersicum (tomato)Positive and negative results

54 papers: 51 positive, 3 negative or no effect

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loss of function · disease · Solanum lycopersicum (tomato)Positive and negative results

155 papers: 63 positive, 92 negative or no effect

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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.