Filamentous sieve element proteins are able to limit phloem mass flow, but not phytoplasma spread

Pagliari, Laura; Buoso, Sara; Santi, Simonetta; Furch, Alexandra C. U.; Martini, Marta; Degola, Francesca; Loschi, Alberto; Bel, Aart J. E. van; Musetti, Rita

doi:10.1093/jxb/erx199

Cited by 36 publications

(59 citation statements)

References 74 publications

(131 reference statements)

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“…Recently, we demonstrated that phloem flow was limited in Chrysanthemum yellows (CY) phytoplasmainfected wild-type plants, but not in healthy wild-type and neither in healthy and infected Atseor mutant lines. Moreover, phloem flow reduction and CY phytoplasma dissemination did not seem to be correlated, since the phytoplasma titre was significantly lower in the mutant line Atseor1ko than in wild-type plants (95.55E+06 and 600.87E+06 phytoplasma genome units mg -1 of leaf sample, respectively) 12 . This phenomenon could be explained by the assumption that phytoplasmas are not passively translocated by phloem mass flow and, hence, do not strictly depend on mass flow for their spread 13 .…”

Section: Sieve-tube Constriction Does Not Limit Phytoplasma Spreadmentioning

confidence: 92%

What Slows Down Phytoplasma Proliferation? Speculations on the Involvement of AtSEOR2 Protein in Plant Defence Signalling

Pagliari

Buoso

Santi

et al. 2018

Plant Signaling & Behavior

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Considering the crude methods used to control phytoplasma diseases, a deeper knowledge on the defence mechanisms recruited by the plant to face phytoplasma invasion is required. Recently, we demonstrated that Arabidopsis mutants lacking AtSEOR1 gene showed a low phytoplasma titre. In wild type plants AtSEOR1 and AtSEOR2 are tied in filamentous proteins. Knockout of the AtSEOR1 gene may pave the way for an involvement of free AtSEOR2 proteins in defence mechanisms. Among the proteins conferring resistance against pathogenic bacteria, AtRPM1-interacting protein has been found to interact with AtSEOR2 in a high-quality, matrix-based yeast-two hybrid assay. For this reason, we investigated the expression levels of Arabidopsis AtRIN4, and the associated AtRPM1 and AtRPS2 genes in healthy and Chrysanthemum yellows-infected wild-type and Atseor1ko lines.

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Section: Sieve-tube Constriction Does Not Limit Phytoplasma Spreadmentioning

confidence: 92%

What Slows Down Phytoplasma Proliferation? Speculations on the Involvement of AtSEOR2 Protein in Plant Defence Signalling

Pagliari

Buoso

Santi

et al. 2018

Plant Signaling & Behavior

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“…Sieve-element protein filaments aggregate in sieve tubes of wild-type Arabidopsis line from the early stage of infection onward. We previously demonstrated that SE protein filaments play a role in the plant response to phytoplasma infection, even in the absence of genes that are considered necessary for their formation in healthy plants 8,9 . Nevertheless, the picture drawn at that time did not explain whether SE protein filaments per se are involved in some defence mechanisms, such as early pathogen containment.…”

Section: Discussionmentioning

confidence: 99%

“…For phytoplasma detection, the 3 insects used on each Arabidopsis were pooled, to obtain 72 pools per condition. Total DNA was extracted as described 79 and the presence of phytoplasmas in each pool was assayed by conventional PCR using the primer pair R16F2/R2, as described by Pagliari and co-authors 9 .…”

Section: Methodsmentioning

confidence: 99%

“…Total DNA was extracted from 200 mg of whole-leaf tissue of H-Ev and CY-Ev plants according to Martini et al 80 . The amount of CY phytoplasmas was quantified according to a real-time PCR protocol described in detail by Pagliari and co-authors 9 . Briefly, the ribosomal protein gene rplV (rpl22) was the target for amplification of CY phytoplasma DNA using the primer pair rp(I-B) F2/rp(I-B)R2 9 ) and a CFX96 real-time PCR detection system (Bio-Rad Laboratories, Richmond, CA, USA).…”

Section: Methodsmentioning

confidence: 99%

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Pre-symptomatic modified phytohormone profile is associated with lower phytoplasma titres in an Arabidopsis seor1ko line

Bernardini

Pagliari

Rosa

et al. 2020

Sci Rep

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The proteins AtSEOR1 and AtSEOR2 occur as conjugates in the form of filaments in sieve elements of Arabidopsis thaliana. A reduced phytoplasma titre found in infected defective-mutant Atseor1ko plants in previous work raised the speculation that non-conjugated SEOR2 is involved in the phytohormone-mediated suppression of Chrysanthemum Yellows (CY)-phytoplasma infection transmitted by Euscelidius variegatus (Ev). This early and long-lasting SEOR2 impact was revealed in Atseor1ko plants by the lack of detectable phytoplasmas at an early stage of infection (symptomless plants) and a lower phytoplasma titre at a later stage (fully symptomatic plants). The high insect survival rate on Atseor1ko line and the proof of phytoplasma infection at the end of the acquisition access period confirmed the high transmission efficiency of CY-phytoplasma by the vectors. Transmission electron microscopy analysis ruled out a direct role of SE filament proteins in physical phytoplasma containment. Time-correlated HPLC–MS/MS-based phytohormone analyses revealed increased jasmonate levels in midribs of Atseor1ko plants at an early stage of infection and appreciably enhanced levels of indole acetic acid and abscisic acid at the early and late stages. Effects of Ev-probing on phytohormone levels was not found. The results suggest that SEOR2 interferes with phytohormonal pathways in Arabidopsis midrib tissues in order to establish early defensive responses to phytoplasma infection.

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“…SEO proteins are widespread and likely ubiquitous among dicotyledon plants (Rüping et al, 2010;Ernst et al, 2011). In most dicotyledonous plants, SEO proteins are believed to be filamentous and confined to a parietal position in translocating sieve elements (Ehlers et al, 2000;Froleich et al, 2011;Anstead et al, 2012;Pagliari et al, 2017). Upon damage, they are released into the lumen of the sieve element and are carried to the downstream sieve plate where they occlude the sieve pores (Ehlers et al, 2000;Ernst et al, 2012;Jekat et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

Sieve element occlusion provides resistance against Aphis gossypii in TGR‐1551 melons

Peng

Walker

2018

Insect Science

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Feeding behavior and plant response to feeding were studied for the aphid Aphis gossypii Glover on susceptible and resistant melons (cv. Iroquois and TGR-1551, respectively). Average phloem phase bout duration on TGR-1551 was <7% of the duration on Iroquois. Sixty-seven percent of aphids on TGR-1551 never produced a phloem phase that attained ingestion (EPG waveform E2) in contrast to only 7% of aphids on Iroquois. Average bout duration of waveform E2 (scored as zero if phloem phase did not attain E2) on TGR-1551 was <3% of the duration on Iroquois. Conversely, average bout duration of EPG waveform E1 (sieve element salivation) was 2.8 times greater on TGR-1551 than on Iroquois. In a second experiment, liquid nitrogen was used to rapidly cryofix leaves and aphids within a few minutes after the aphids penetrated a sieve element. Phloem near the penetration site was then examined by confocal laser scanning microscopy. Ninety-six percent of penetrated sieve elements were occluded by protein in TGR-1551 in contrast to only 28% in Iroquois. Usually in TGR-1551, occlusion was also observed in nearby nonpenetrated sieve elements. Next, a calcium channel blocker, trivalent lanthanum, was used to prevent phloem occlusion in TGR-1551, and A. gossypii feeding behavior and the plant's phloem response were compared between lanthanum-treated and control TGR-1551. Lanthanum treatment eliminated the sieve element protein occlusion response and the aphids readily ingested phloem sap from treated plants. This study provides strong evidence that phloem occlusion is a mechanism for resistance against A. gossypii in TGR-1551.

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Filamentous sieve element proteins are able to limit phloem mass flow, but not phytoplasma spread

Abstract: The lack of correlation between sieve element filament formation, sieve element occlusion, and phytoplasma titre hints at an unknown role for filamentous sieve element proteins in plant defence.

Cited by 36 publications

References 74 publications

What Slows Down Phytoplasma Proliferation? Speculations on the Involvement of AtSEOR2 Protein in Plant Defence Signalling

What Slows Down Phytoplasma Proliferation? Speculations on the Involvement of AtSEOR2 Protein in Plant Defence Signalling

Pre-symptomatic modified phytohormone profile is associated with lower phytoplasma titres in an Arabidopsis seor1ko line

Sieve element occlusion provides resistance against Aphis gossypii in TGR‐1551 melons

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