Paper · 2023 · Phytopathology

Phloem and Xylem Responses Are Both Implicated in Huanglongbing Tolerance of Sugar Belle

Jacobo Robledo; Stacy Welker; Ilana Shtein; et al.

14
claims
35
verbatim quotes
5
citations
5
research areas
—
Not open access

Abstract

Although huanglongbing (HLB) is a devastating citrus disease, improved tolerant cultivars, such as Sugar Belle (SB) mandarin, have been identified. To understand the responses that HLB-affected SB undergoes, we compared 14 CO 2 fixation, carbohydrate export, phloem callose accumulation, relative expression of plant defense activators, and anatomical changes between healthy and infected SB trees versus susceptible Pineapple (PA) sweet orange. Eight- to ten-week-old leaves of infected SB showed a 2.5-fold increase in 14 CO 2 fixation and a 13% decrease in 14 C-carbohydrate export, whereas HLB-affected PA presented a decrease of 33 and 50%, respectively. The mean distance of a callose deposit to its closest neighbor was 36% smaller in infected SB versus healthy, whereas in HLB-affected PA, it was 33% higher. Expression of papain-like cysteine proteases (PLCPs) was upregulated in SB but downregulated in PA. Infected SB showed minor alterations in the number of xylem vessels, a 16% larger xylem vessel lumen area, and a 14% increase in the proportional area of the xylem. In contrast, PA showed a 2.4-fold increase in the xylem vessel number and a 2% increase in the proportional xylem area. Three complementary mechanisms of tolerance in SB are hypothesized: (i) increased carbohydrate availability induced by greater CO 2 fixation, mild effect in carbohydrate export, and local accumulation of callose in the phloem; (ii) activation of defense response via upregulation of PLCPs, and (iii) increased investment in the xylem structure. Thus, phloem and xylem modifications seem to be involved in SB tolerance.

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Claims 14

Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Infected SB leaves had a 2.5-fold increase in carbon fixation.

Taxon
Sugar Bellee1
Material
SBe0
Organ / stage
Eight- to ten-week-old leavese0
Treatment
infectede0
Outcome
14 CO 2 fixatione0
Direction
increasee0
Value
2.5-folde0

Verbatim

e0

“Eight- to ten-week-old leaves of infected SB showed a 2.5-fold increase in 14 CO 2 fixation”

✓ located verbatim in the source · abstract, characters 446–537 · show in text ↑
e1

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Infected SB leaves had a 13% decrease in carbohydrate export.

Taxon
Sugar Bellee2
Organ / stage
Eight- to ten-week-old leavese1
Outcome
14 C-carbohydrate exporte0
Direction
decreasee0
Value
13%e0

Verbatim

e0

“a 13% decrease in 14 C-carbohydrate export”

✓ located verbatim in the source · abstract, characters 542–584 · show in text ↑
e1

“Eight- to ten-week-old leaves of infected SB”

✓ located verbatim in the source · abstract, characters 446–490 · show in text ↑
e2

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

HLB-affected PA had a 33% decrease in carbon fixation.

Taxon
PineappleAnanas comosuse2
Outcome
14 CO 2 fixatione1
Direction
decreasee0
Value
33e0
Qualifier
HLB-affectede0

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

Ananas comosus
Ananas comosus · TaxonVpuipV ,pemegang hak cipta · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“HLB-affected PA presented a decrease of 33 and 50%, respectively”

✓ located verbatim in the source · abstract, characters 594–658 · show in text ↑
e1

“14 CO 2 fixation and a 13% decrease in 14 C-carbohydrate export”

✓ located verbatim in the source · abstract, characters 521–584 · show in text ↑
e2

“Pineapple (PA) sweet orange”

✓ located verbatim in the source · abstract, characters 417–444 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

HLB-affected PA had a 50% decrease in carbohydrate export.

Taxon
PineappleAnanas comosuse2
Outcome
14 C-carbohydrate exporte1
Direction
decreasee0
Value
50%e0

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

Ananas comosus
Ananas comosus · TaxonVpuipV ,pemegang hak cipta · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“HLB-affected PA presented a decrease of 33 and 50%, respectively”

✓ located verbatim in the source · abstract, characters 594–658 · show in text ↑
e1

“14 C-carbohydrate export”

✓ located verbatim in the source · abstract, characters 560–584 · show in text ↑
e2

“Pineapple (PA) sweet orange”

✓ located verbatim in the source · abstract, characters 417–444 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Nearest-neighbor callose deposit distance was 36% smaller in infected SB.

Taxon
Sugar Bellee1
Outcome
mean distance of a callose deposit to its closest neighbore0
Direction
smallere0
Value
36%e0
Comparator
healthye0

Verbatim

e0

“The mean distance of a callose deposit to its closest neighbor was 36% smaller in infected SB versus healthy”

✓ located verbatim in the source · abstract, characters 660–768 · show in text ↑
e1

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Nearest-neighbor callose deposit distance was 33% higher in HLB-affected PA.

Taxon
PineappleAnanas comosuse2
Outcome
mean distance of a callose deposit to its closest neighbore1
Direction
highere0
Value
33%e0

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

Ananas comosus
Ananas comosus · TaxonVpuipV ,pemegang hak cipta · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“in HLB-affected PA, it was 33% higher”

✓ located verbatim in the source · abstract, characters 778–815 · show in text ↑
e1

“The mean distance of a callose deposit to its closest neighbor”

✓ located verbatim in the source · abstract, characters 660–722 · show in text ↑
e2

“Pineapple (PA) sweet orange”

✓ located verbatim in the source · abstract, characters 417–444 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

PLCP expression rose in SB.

Taxon
Sugar Bellee1
Gene
papain-like cysteine proteases (PLCPs)e0
Outcome
Expression of papain-like cysteine proteases (PLCPs)e0
Direction
upregulatede0

Verbatim

e0

“Expression of papain-like cysteine proteases (PLCPs) was upregulated in SB”

✓ located verbatim in the source · abstract, characters 817–891 · show in text ↑
e1

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

PLCP expression fell in PA.

Taxon
PineappleAnanas comosuse1
Gene
papain-like cysteine proteases (PLCPs)e0
Outcome
Expression of papain-like cysteine proteases (PLCPs)e0
Direction
downregulatede0

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

Ananas comosus
Ananas comosus · TaxonVpuipV ,pemegang hak cipta · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“Expression of papain-like cysteine proteases (PLCPs) was upregulated in SB but downregulated in PA”

✓ located verbatim in the source · abstract, characters 817–915 · show in text ↑
e1

“Pineapple (PA) sweet orange”

✓ located verbatim in the source · abstract, characters 417–444 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

Infected SB showed minor changes in xylem vessel number.

Taxon
Sugar Bellee1
Outcome
number of xylem vesselse0
Direction
minor alterationse0

Verbatim

e0

“Infected SB showed minor alterations in the number of xylem vessels”

✓ located verbatim in the source · abstract, characters 917–984 · show in text ↑
e1

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Infected SB had a 16% larger xylem vessel lumen area.

Taxon
Sugar Bellee2
Outcome
xylem vessel lumen areae0
Direction
largere0
Value
16%e0

Verbatim

e0

“a 16% larger xylem vessel lumen area”

✓ located verbatim in the source · abstract, characters 986–1022 · show in text ↑
e1

“Infected SB showed minor alterations”

✓ located verbatim in the source · abstract, characters 917–953 · show in text ↑
e2

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultpositivemeasured

Claim · model-written summary

Infected SB had a 14% increase in proportional xylem area.

Taxon
Sugar Bellee2
Outcome
proportional area of the xyleme0
Direction
increasee0
Value
14%e0

Verbatim

e0

“a 14% increase in the proportional area of the xylem”

✓ located verbatim in the source · abstract, characters 1028–1080 · show in text ↑
e1

“Infected SB showed minor alterations”

✓ located verbatim in the source · abstract, characters 917–953 · show in text ↑
e2

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

PA had a 2.4-fold increase in xylem vessel number.

Taxon
PineappleAnanas comosuse1
Outcome
xylem vessel numbere0
Direction
increasee0
Value
2.4-folde0

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

Ananas comosus
Ananas comosus · TaxonVpuipV ,pemegang hak cipta · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“PA showed a 2.4-fold increase in the xylem vessel number”

✓ located verbatim in the source · abstract, characters 1095–1151 · show in text ↑
e1

“Pineapple (PA) sweet orange”

✓ located verbatim in the source · abstract, characters 417–444 · show in text ↑
Observationobservedoriginal resultmeasured

Claim · model-written summary

PA had a 2% increase in proportional xylem area.

Taxon
PineappleAnanas comosuse2
Outcome
proportional xylem areae0
Direction
increasee0
Value
2%e0

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

Ananas comosus
Ananas comosus · TaxonVpuipV ,pemegang hak cipta · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“a 2% increase in the proportional xylem area”

✓ located verbatim in the source · abstract, characters 1156–1200 · show in text ↑
e1

“PA showed a 2.4-fold increase”

✓ located verbatim in the source · abstract, characters 1095–1124 · show in text ↑
e2

“Pineapple (PA) sweet orange”

✓ located verbatim in the source · abstract, characters 417–444 · show in text ↑
Mechanismhypothesisoriginal resultpositivebasis n/a

Claim · model-written summary

The authors hypothesize that carbohydrate availability, defense activation and xylem investment contribute to SB tolerance.

Taxon
Sugar Bellee1
Outcome
tolerance in SBe0
Qualifier
increased carbohydrate availabilitye0

Verbatim

e0

“Three complementary mechanisms of tolerance in SB are hypothesized: (i) increased carbohydrate availability induced by greater CO 2 fixation, mild effect in carbohydrate export, and local accumulation of callose in the phloem; (ii) activation of defense response via upregulation of PLCPs, and (iii) increased investment in the xylem structure”

✓ located verbatim in the source · abstract, characters 1202–1545 · show in text ↑
e1

“Sugar Belle (SB) mandarin”

✓ located verbatim in the source · abstract, characters 99–124 · show in text ↑