Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato

Albacete, Alfonso; Cantero-Navarro, Elena; Großkinsky, Dominik K.; Arias, Cintia L.; Balibrea, María E.; Bru, Roque; Fragner, Lena; Ghanem, Michel Edmond; González, María de la Cruz; Hernández, José Antonio; Martínez‐Andújar, Cristina; Graaff, Eric van der; Weckwerth, Wolfram; Zellnig, Günther; Pérez‐Alfocea, Francisco; Roitsch, Thomas

doi:10.1093/jxb/eru448

Cited by 73 publications

(34 citation statements)

References 77 publications

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“…In this study, the expression level of VINV was dramatically higher in the tetraploid than in the diploid under both non‐stressed and drought conditions. Increased levels of INV has been reported to act as a part of the stress response in a variety of plant species (Albacete et al ., ; Dahro et al ., ; Koonjul et al ., ; Mišić et al ., ). It is noted that sucrose content was reduced in the tetraploid, concomitant with an increase in glucose content, relative to the diploid, implying that the higher levels of glucose in the tetraploid might contribute to the enhanced drought tolerance.…”

Section: Discussionmentioning

confidence: 97%

Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata

Wei

Wang

Xie

et al. 2019

Plant Biotechnology Journal

115

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Summary Tetraploids have been reported to exhibit increased stress tolerance, but the underlying molecular and physiological mechanisms remain poorly understood. In this study, autotetraploid plants were identified by screening natural seedlings of trifoliate orange ( Poncirus trifoliata ). The tetraploids exhibited different morphology and displayed significantly enhanced drought and dehydration tolerance in comparison with the diploid progenitor. Transcriptome analysis indicated that a number of stress‐responsive genes and pathways were differentially influenced and enriched in the tetraploids, in particular those coding for enzymes related to antioxidant process and sugar metabolism. Transcript levels and activities of antioxidant enzymes (peroxidase and superoxide dismutase) and sucrose‐hydrolysing enzyme (vacuolar invertase) were increased in the tetraploids upon exposure to the drought, concomitant with greater levels of glucose but lower level of reactive oxygen species ( ROS ). These data indicate that the tetraploids might undergo extensive transcriptome reprogramming of genes involved in ROS scavenging and sugar metabolism, which contributes, synergistically or independently, to the enhanced stress tolerance of the tetraploid. Our results reveal that the tetraploids take priority over the diploid for stress tolerance by maintaining a more robust system of ROS detoxification and osmotic adjustment via elevating antioxidant capacity and sugar accumulation in comparison with the diploid counterpart.

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Section: Discussionmentioning

confidence: 97%

Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata

Wei

Wang

Xie

et al. 2019

Plant Biotechnology Journal

115

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“…The role of cytoplasmic neutral invertases remains unclear. They seem to play a role in the antioxidant system involved in cellular reactive oxygen species homeostasis and they have been shown to be involved in responses to abiotic stresses (Albacete et al ., , ; Chen et al ., ; Liu et al ., ; Xu et al ., ). We have shown a strong connectivity between several genes related to sugar metabolism.…”

Section: Discussionmentioning

confidence: 99%

Allele‐specific expression and genetic determinants of transcriptomic variations in response to mild water deficit in tomato

et al. 2018

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Characterizing the natural diversity of gene expression across environments is an important step in understanding how genotype-by-environment interactions shape phenotypes. Here, we analyzed the impact of water deficit onto gene expression levels in tomato at the genome-wide scale. We sequenced the transcriptome of growing leaves and fruit pericarps at cell expansion stage in a cherry and a large fruited accession and their F hybrid grown under two watering regimes. Gene expression levels were steadily affected by the genotype and the watering regime. Whereas phenotypes showed mostly additive inheritance, ~80% of the genes displayed non-additive inheritance. By comparing allele-specific expression (ASE) in the F hybrid to the allelic expression in both parental lines, respectively, 3005 genes in leaf and 2857 genes in fruit deviated from 1:1 ratio independently of the watering regime. Among these genes, ~55% were controlled by cis factors, ~25% by trans factors and ~20% by a combination of both types of factors. A total of 328 genes in leaf and 113 in fruit exhibited significant ASE-by-watering regime interaction, among which ~80% presented trans-by-watering regime interaction, suggesting a response to water deficit mediated through a majority of trans-acting loci in tomato. We cross-validated the expression levels of 274 transcripts in fruit and leaves of 124 recombinant inbred lines (RILs) and identified 163 expression quantitative trait loci (eQTLs) mostly confirming the divergences identified by ASE. Combining phenotypic and expression data, we observed a complex network of variation between genes encoding enzymes involved in the sugar metabolism.

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“…Under abiotic conditions, the constant induction of PtC/VIF1 transcript upon drought and wound in the roots suggested that it was dehydration-and wound-responsive gene. Recently, promising work in tomato revealed that significant elevation of CWI activities rather than the transcripts conferred the improvement of drought tolerance (Albacete et al, 2015), reflecting the roles of CIF in the post-translational regulation. Suppression of a tomato CIF expression can significantly delay the leaf senescence and fruit size (Jin et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…The promotions of CWI on seed filling and fruit set have been well attempted in a wide range of plant species like maize, rice, tomato, cotton, and litchi (Chourey et al, 2006;Wang et al, 2008;Zanor et al, 2009;Wang and Ruan, 2012;Li et al, 2013;Zhang et al, 2018), indicating that CWIs facilitate the improvement of sink cell differentiation via multiple regulatory mechanisms of sugar metabolism and signaling. Recently, overexpressing CWIs in tobacco and tomato resulted in the deferral of leaf aging and drought avoidance (Balibrea Lara et al, 2004;Albacete et al, 2015). Also numerous reports also revealed that CWI plays central roles in defense and immune responses during plants-pathogen interactions (Swarbrick et al, 2006;Essmann et al, 2008;Kocal et al, 2008;Sun et al, 2014;Veillet et al, 2016), pointing out that CWI serves as a significant stress indicator and pathogenesis-related proteins.…”

Section: Introductionmentioning

confidence: 99%

Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa

Han

Min

et al. 2020

Front. Plant Sci.

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In higher plants, cell wall invertase (CWI) and vacuolar invertase (VI) were considered to be essential coordinators in carbohydrate partitioning, sink strength determination, and stress responses. An increasing body of evidence revealed that the tight regulation of CWI and VI substantially depends on the post-translational mechanisms, which were mediated by small proteinaceous inhibitors (C/VIFs, Inhibitor of b-Fructosidases). As yet, the extensive survey of the molecular basis and biochemical property of C/VIFs remains largely unknown in black cottonwood (Populus trichocarpa Torr. & A. Gray), a model species of woody plants. In the present work, we have initiated a systematic review of the genomic structures, phylogenies, cis-regulatory elements, and conserved motifs as well as the tissue-specific expression, resulting in the identification of 39 genes encoding C/VIF in poplar genome. We characterized two putative invertase inhibitors PtC/VIF1 and 2, showing predominant transcript levels in the roots and highly divergent responses to the selected stress cues including fusarium wilt, drought, ABA, wound, and senescence. In silico prediction of the signal peptide hinted us that they both likely had the apoplastic targets. Based on the experimental visualization via the transient and stable transformation assays, we confirmed that PtC/VIF1 and 2 indeed secreted to the extracellular compartments. Further validation of their recombinant enzymes revealed that they displayed the potent inhibitory affinities on the extracted CWI, supporting the patterns that act as the typical apoplastic invertase inhibitors. To our knowledge, it is the first report on molecular characterization of the functional C/VIF proteins in poplar. Our results indicate that PtC/VIF1 and 2 may exert essential roles in defense-and stress-related responses. Moreover, novel findings of the up-and downregulated C/VIF genes and functional enzyme activities enable us to further unravel the molecular mechanisms in the promotion of woody plant performance and adaptedbiotic stress, underlying the homeostatic control of sugar in the apoplast.

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Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato

Abstract: HighlightOverexpression of a cell wall invertase gene promotes dehydration avoidance and WUE, and delays senescence in tomato through limiting stomatal conductance and inducing sink metabolism and photosynthesis in source leaves.

Cited by 73 publications

References 77 publications

Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata

Enhanced ROS scavenging and sugar accumulation contribute to drought tolerance of naturally occurring autotetraploids in Poncirus trifoliata

Allele‐specific expression and genetic determinants of transcriptomic variations in response to mild water deficit in tomato

Functional Characterization of Invertase Inhibitors PtC/VIF1 and 2 Revealed Their Involvements in the Defense Response to Fungal Pathogen in Populus trichocarpa

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