Silencing polygalacturonase expression inhibits tomato petiole abscission

Jiang, Cai‐Zhong; Feng, Lu; Imsabai, Wachiraya; Meir, Shimon; Reid, Michael S.

doi:10.1093/jxb/ern023

Cited by 92 publications

(75 citation statements)

References 24 publications

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“…In addition, Jiang et al (2008) have recently shown that PGs are also involved in leaf abscission in tomato. Taken together, these results support the conclusion that multiple, and possibly all, cell separation/ abscission/dehiscence events in plants use a common PGdependent mechanism.…”

Section: Discussionmentioning

confidence: 99%

“…Although there is only limited direct genetic evidence for the physiological importance of individual PGs, correlations have been reported between increasing PG activity and cell separation in fruit ripening and in the shedding of leaves, flowers, and fruit (Taylor et al, 1993;Kalaitzis et al, 1995;Brown, 1997;Kalaitzis et al, 1997). More recently, silencing of tomato (Solanum lycopersicum) abscission-related PGs was shown to increase the break strength of the leaf abscission zone and delay abscission in explants treated with ethylene (Jiang et al, 2008), and a putative Arabidopsis PG has been shown to promote floral organ abscission (Gonzá lezCarranza et al, 2007). The importance of PG is also illustrated by the 'Flavr savr' tomato and peach (Prunus persica) lacking a functional Melting flesh/Freestone locus (Peace et al, 2005), both of which have reduced expression of a fruit ripening-associated PG and delayed fruit softening.…”

Section: Introductionmentioning

confidence: 99%

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ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 Are Polygalacturonases Required for Cell Separation during Reproductive Development inArabidopsis

et al. 2009

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Cell separation is thought to involve degradation of pectin by several hydrolytic enzymes, particularly polygalacturonase (PG). Here, we characterize an activation tagging line with reduced growth and male sterility caused by increased expression of a PG encoded by QUARTET2 (QRT2). QRT2 is essential for pollen grain separation and is part of a small family of three closely related endo-PGs in the Arabidopsis thaliana proteome, including ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1) and ADPG2. Functional assays and complementation experiments confirm that ADPG1, ADPG2, and QRT2 are PGs. Genetic analysis demonstrates that ADPG1 and ADPG2 are essential for silique dehiscence. In addition, ADPG2 and QRT2 contribute to floral organ abscission, while all three genes contribute to anther dehiscence. Expression analysis is consistent with the observed mutant phenotypes. INDEHISCENT (IND) encodes a putative basic helix-loop-helix required for silique dehiscence, and we demonstrate that the closely related HECATE3 (HEC3) gene is required for normal seed abscission and show that IND and HEC3 are required for normal expression of ADPG1 in the silique dehiscence zone and seed abscission zone, respectively. We also show that jasmonic acid and ethylene act together with abscisic acid to regulate floral organ abscission, in part by promoting QRT2 expression. These results demonstrate that multiple cell separation events, including both abscission and dehiscence, require closely related PG genes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 Are Polygalacturonases Required for Cell Separation during Reproductive Development inArabidopsis

et al. 2009

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“…Inhibition of the PG gene expression results in inhibition of abscission and dehiscence (Jiang et al, 2008;Ogawa et al, 2009). Cellulases are also thought to be involved in cell wall degradation during abscission, and inhibition of the tomato cellulase gene expression results in partial inhibition of abscission (Lashbrook et al, 1998;Brummell et al, 1999).…”

Section: Abscission Is Impeded In Transgenic Plants Overexpressing Anmentioning

confidence: 99%

“…In many cases, the abscission process is induced by ethylene, while the rate and degree of abscission depends upon the endogenous balance between auxin and ethylene levels in the tissue (Patterson, 2001;Taylor and Whitelaw, 2001;Roberts et al, 2002;Meir et al, 2006Meir et al, , 2010: Auxin concentrations must be reduced in the AZ to render it sensitive to ethylene, which promotes the advancement of abscission (Abeles and Rubinstein, 1964;Sexton and Roberts, 1982). Based on expression patterns and modulation in transgenic plants and mutants, genes encoding polygalacturonases (PGs) and b-1,4-glucanases (cellulases) have been suggested to play a central role in the execution of cell separation (Greenberg et al, 1975;Lashbrook et al, 1998;Brummell et al, 1999;Hong et al, 2000;Gonzá lez-Carranza et al, 2007;Jiang et al, 2008;Ogawa et al, 2009). Other proteins associated with the AZ are expansin (Cho and Cosgrove, 2000;Belfield et al, 2005), pathogenesis-related proteins (Eyal et al, 1993;Coupe et al, 1997), and metallothioneins (Coupe et al, 1995), but their role in the process is not yet clear.…”

Section: Introductionmentioning

confidence: 99%

Programmed Cell Death Occurs Asymmetrically during Abscission in Tomato

et al. 2011

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Abscission occurs specifically in the abscission zone (AZ) tissue as a natural stage of plant development. Previously, we observed delay of tomato (Solanum lycopersicum) leaf abscission when the LX ribonuclease (LX) was inhibited. The known association between LX expression and programmed cell death (PCD) suggested involvement of PCD in abscission. In this study, hallmarks of PCD were identified in the tomato leaf and flower AZs during the late stage of abscission. These included loss of cell viability, altered nuclear morphology, DNA fragmentation, elevated levels of reactive oxygen species and enzymatic activities, and expression of PCD-associated genes. Overexpression of antiapoptotic proteins resulted in retarded abscission, indicating PCD requirement. PCD, LX, and nuclease gene expression were visualized primarily in the AZ distal tissue, demonstrating an asymmetry between the two AZ sides. Asymmetric expression was observed for genes associated with cell wall hydrolysis, leading to AZ, or associated with ethylene biosynthesis, which induces abscission. These results suggest that different abscission-related processes occur asymmetrically between the AZ proximal and distal sides. Taken together, our findings identify PCD as a key mechanism that occurs asymmetrically during normal progression of abscission and suggest an important role for LX in this PCD process.

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“…Recently, the use of internal markers for VIGS based on pigment accumulation in petunia (Petunia hybrida), soybean (Glycine max), and tomato has proven very successful for empowering the method as a reverse genetics tool (Chen et al, 2004b;Nagamatsu et al, 2007;Spitzer et al, 2007;Jiang et al, 2008). Tomato introgression lines accumulating anthocyanins in their fruit have been described, but this accumulation is restricted to the epidermis; therefore, the use of these lines is restricted to analysis of gene function in this tissue.…”

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confidence: 99%

A Visual Reporter System for Virus-Induced Gene Silencing in Tomato Fruit Based on Anthocyanin Accumulation

et al. 2009

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Innes Centre, Colney, Norwich NR4 7UH, United Kingdom (E.B., C.M.)Virus-induced gene silencing (VIGS) is a powerful tool for reverse genetics in tomato (Solanum lycopersicum). However, the irregular distribution of the effects of VIGS hampers the identification and quantification of nonvisual phenotypes. To overcome this limitation, a visually traceable VIGS system was developed for fruit, comprising two elements: (1) a transgenic tomato line (Del/Ros1) expressing Antirrhinum majus Delila and Rosea1 transcription factors under the control of the fruitspecific E8 promoter, showing a purple-fruited, anthocyanin-rich phenotype; and (2) a modified tobacco rattle virus VIGS vector incorporating partial Rosea1 and Delila sequences, which was shown to restore the red-fruited phenotype upon agroinjection in Del/Ros1 plants. Dissection of silenced areas for subsequent chemometric analysis successfully identified the relevant metabolites underlying gene function for three tomato genes, phytoene desaturase, TomloxC, and SlODO1, used for proof of concept. The C-6 aldehydes derived from lipid 13-hydroperoxidation were found to be the volatile compounds most severely affected by TomloxC silencing, whereas geranial and 6-methyl-5-hepten-2-one were identified as the volatiles most severely reduced by phytoene desaturase silencing in ripening fruit. In a third example, silencing of SlODO1, a tomato homolog of the ODORANT1 gene encoding a myb transcription factor, which regulates benzenoid metabolism in petunia (Petunia hybrida) flowers, resulted in a sharp accumulation of benzaldehyde in tomato fruit. Together, these results indicate that fruit VIGS, enhanced by anthocyanin monitoring, can be a powerful tool for reverse genetics in the study of the metabolic networks operating during fruit ripening.

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Silencing polygalacturonase expression inhibits tomato petiole abscission

Cited by 92 publications

References 24 publications

ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 Are Polygalacturonases Required for Cell Separation during Reproductive Development inArabidopsis

ARABIDOPSIS DEHISCENCE ZONE POLYGALACTURONASE1 (ADPG1), ADPG2, and QUARTET2 Are Polygalacturonases Required for Cell Separation during Reproductive Development inArabidopsis

Programmed Cell Death Occurs Asymmetrically during Abscission in Tomato

A Visual Reporter System for Virus-Induced Gene Silencing in Tomato Fruit Based on Anthocyanin Accumulation

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