Functional Characterization of a Drought-Responsive Invertase Inhibitor from Maize (Zea mays L.)

Chen, Lin; Liu, Xiaohong; Huang, Xiaodan; Luo, Wei; Long, Yuming; Greiner, Steffen; Rausch, Thomas; Zhao, Hongbo

doi:10.3390/ijms20174081

Cited by 11 publications

(12 citation statements)

References 36 publications

(52 reference statements)

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“…TBtools (https://www.biorxiv.org/content/10.1101/289660v3, accessed on 3 June 2019) was used to visualize the expression of the candidate genes. For the quantitative real-time PCR (qPCR) analysis, RNA extraction and cDNA synthesis were performed according to the methods described in a previous report [55]. An additional step was performed with the Rotor-Gene 3000 system using SYBR Premix ExTaq II (Takara, Shiga, Japan) to monitor dsDNA synthesis.…”

Section: Transcriptomic Sequencing and Gene Expression Analysismentioning

confidence: 99%

Functional Characterization of a Cucumber (Cucumis sativus L.) Vacuolar Invertase, CsVI1, Involved in Hexose Accumulation and Response to Low Temperature Stress

Feng

Zheng

et al. 2021

IJMS

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Cucumber (Cucumis sativus L.), an important vegetable plant species, is susceptible to low temperature stress especially during the seedling stage. Vacuolar invertase (VI) plays important roles in plant responses to abiotic stress. However, the molecular and biochemical mechanisms of VI function in cucumber, have not yet been completely understood and VI responses to low temperature stress and it functions in cold tolerance in cucumber seedlings are also in need of exploration. The present study found that hexose accumulation in the roots of cucumber seedlings under low temperature stress is closely related to the observed enhancement of invertase activity. Our genome-wide search for the vacuolar invertase (VI) genes in cucumber identified the candidate VI-encoding gene CsVI1. Expression profiling of CsVI1 showed that it was mainly expressed in the young roots of cucumber seedlings. In addition, transcriptional analysis indicated that CsVI1 expression could respond to low temperature stress. Recombinant CsVI1 proteins purified from Pichia pastoris and Nicotiana benthamiana leaves could hydrolyze sucrose into hexoses. Further, overexpression of CsVI1 in cucumber plants could increase their hexose contents and improve their low temperature tolerance. Lastly, a putative cucumber invertase inhibitor was found could form a complex with CsVI1. In summary, these results confirmed that CsVI1 functions as an acid invertase involved in hexose accumulation and responds to low temperature stress in cucumber seedlings.

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Section: Transcriptomic Sequencing and Gene Expression Analysismentioning

confidence: 99%

Functional Characterization of a Cucumber (Cucumis sativus L.) Vacuolar Invertase, CsVI1, Involved in Hexose Accumulation and Response to Low Temperature Stress

Feng

Zheng

et al. 2021

IJMS

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“…Previous studies have obtained inconsistent results in terms of the correlation between invertase activity and ovary abortion in ovaries, and this may be related to the stage when treatments are applied. Changes in CWI activity under drought stress were found to be related to ovary abortion in some studies ( Boyer, 2004 ; McLaughlin and Boyer, 2004 ; Chen et al, 2019 ), but their treatments began after silks emerged from the bracts and there were no data for silk growth. In another study, the CWI activity changed in both basal and apical ovaries of maize under a moderate drought treatment, but ovary abortion only occurred in apical ovaries ( Oury et al, 2016a ); that treatment began before silk emergence and decreased the number of emerged silks.…”

Section: Discussionmentioning

confidence: 99%

“…Abiotic stress during the flowering period results in early abortion, and the reasons for early grain abortion differ depending on the type and extent of the abiotic stress ( Hütsch et al, 2014 ; Oury et al, 2016b ; Jung et al, 2017 ; Shen et al, 2018 ; Wang et al, 2020 ). Some previous studies found that a decrease in acid invertase activity was associated with limited kernel setting under salt stress ( Hütsch et al, 2014 ), and that changes in CWI activity under drought stress were related to ovary abortion ( Boyer, 2004 ; McLaughlin and Boyer, 2004 ; Chen et al, 2019 ). However, other studies found that, under moderate drought stress during the flowering period, ovary abortion was not determined by changes in sugar concentrations or invertase activity ( Henry et al, 2015 ; Turc and Tardieu, 2018 ).…”

Section: Introductionmentioning

confidence: 99%

Ovary Abortion Induced by Combined Waterlogging and Shading Stress at the Flowering Stage Involves Amino Acids and Flavonoid Metabolism in Maize

et al. 2021

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Maize (Zea mays L.) crops on the North China Plain are often subject to continuous overcast rain at the flowering stage. This causes waterlogging and shading stresses simultaneously and leads to huge yield losses, but the causes of these yield losses remain largely unknown. To explore the factors contributing to yield loss caused by combined waterlogging and shading stress at the flowering stage, we performed phenotypic, physiological, and quasi-targeted metabolomics analyses of maize plants subjected to waterlogging, shading, and combined waterlogging and shading (WS) treatments. Analyses of phenotypic and physiological indexes showed that, compared with waterlogging or shading alone, WS resulted in lower source strength, more severe inhibition of ovary and silk growth at the ear tip, a reduced number of emerged silks, and a higher rate of ovary abortion. Changes in carbon content and enzyme activity could not explain the ovary abortion in our study. Metabolomic analyses showed that the events occurred in ovaries and silks were closely related to abortion, WS forced the ovary to allocate more resources to the synthesis of amino acids involved in the stress response, inhibited the energy metabolism, glutathione metabolism and methionine salvage pathway, and overaccumulation of H2O2. In silks, WS led to lower accumulation levels of specific flavonoid metabolites with antioxidant capacity, and to over accumulation of H2O2. Thus, compared with each single stress, WS more seriously disrupted the normal metabolic process, and resulted more serious oxidative stress in ovaries and silks. Amino acids involved in the stress response in ovaries and specific flavonoid metabolites with antioxidant capacity in silks play important roles during ovary abortion. These results identify novel traits for selection in breeding programs and targets for genome editing to increase maize yield under WS stress.

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“…Since CWI and VI are intrinsically stable enzymes, the regulation of the enzyme activities depends mainly on the post-translational mechanisms that are mediated by the proteinaceous inhibitors (Ruan, 2014). The physiological roles and biotechnology relevance of C/VIF via finetuning of CWI or VI that modulates sugar metabolism and signaling in apoplast or vacuoles have been attempted in a variety of plants (Greiner et al, 1999;Jin et al, 2009;Liu et al, 2013;Qin et al, 2016;Su et al, 2016;Tang et al, 2017;Chen et al, 2019;Zhao et al, 2019). Hitherto, there is very little literature on molecular mechanisms of the functional genes in the model poplar tree owing to the recalcitrance.…”

Section: Discussionmentioning

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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Functional Characterization of a Drought-Responsive Invertase Inhibitor from Maize (Zea mays L.)

Cited by 11 publications

References 36 publications

Functional Characterization of a Cucumber (Cucumis sativus L.) Vacuolar Invertase, CsVI1, Involved in Hexose Accumulation and Response to Low Temperature Stress

Functional Characterization of a Cucumber (Cucumis sativus L.) Vacuolar Invertase, CsVI1, Involved in Hexose Accumulation and Response to Low Temperature Stress

Ovary Abortion Induced by Combined Waterlogging and Shading Stress at the Flowering Stage Involves Amino Acids and Flavonoid Metabolism in Maize

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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