Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean (<i>Glycine max</i>)

Tang, Xiaofei; Su, Tao; Han, Mei Lan K.; Wei, Lai; Wang, Weiwei; Yu, Zhiyuan; Xue, Yongbo; Wei, Hongbin; Du, Yejie; Greiner, Steffen; Rausch, Thomas; Liu, Lijun

doi:10.1093/jxb/erw425

Cited by 52 publications

(70 citation statements)

References 68 publications

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“…By contrast, silencing of CIF expression also facilitated the improvements of seed filling, prolonged leaf green, and cold tolerance in tomato (Jin et al, 2009;Xu et al, 2017), highlighting that the post-translational control is necessary for hexoses to release to sink organs, particularly responding to stressors and phytohormone cues. These results corroborated the findings that the suppression of CIF expression resulted in increased seed production and germination (Su et al, 2016;Tang et al, 2017). An increasing body of evidence supported the notion that the C/ VIF-mediated post-translational modulation of invertase commonly involves multiple cellular processes, metabolic pathways, and molecular regulation.…”

Section: Introductionsupporting

confidence: 81%

“…The previously described C/VIFs (Link et al, 2004;Tang et al, 2017) were collected as queries to search for the homologs in P. trichocarpa genome assembly (3.0) from the JGI gene catalog (Phytozome v12.1, https://phytozome.jgi.doe.gov/pz/portal. html) with the E-value cutoff set as 1e-5 and GenBank (https:// www.ncbi.nlm.nih.gov/).…”

Section: Methodsmentioning

confidence: 99%

“…The analyses of subcellular localization were conducted according to a previous study (Tang et al, 2017). The CDS (stop codon omitted) of PtC/VIF1 and PtC/VIF2 were amplified by PCR using the primers containing the Gateway™ (Invitrogen, Germany) attB1 and attB2 recombinant sites (Supplementary Table S1).…”

Section: Subcellular Localizationsmentioning

confidence: 99%

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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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Section: Introductionsupporting

confidence: 81%

Section: Methodsmentioning

confidence: 99%

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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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“…The change in expression of GmSPS genes in seeds of the three cultivars ( Figure 5E-H) reflected the change in SPS activity ( Figure 4E), which suggests that the four GmSPS homologs acted together to control sucrose synthesis in drought-stressed seeds. Previous studies have reported that loss-of-function invertase mutants had lower invertase activity and thus lower seed weights [51][52][53][54], which indicated that invertase activity had a critical role in the regulation of seed development. The role of SuSy gene was also important for carbon allocation during seed filling, especially when subjected to drought, cold, and heat stress [14,55].…”

Section: Drought Stress Affects Carbohydrate Enrichment and Metabolismentioning

confidence: 96%

Effect of Drought Stress during Soybean R2–R6 Growth Stages on Sucrose Metabolism in Leaf and Seed

Zhao

Chen

et al. 2020

IJMS

110

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Sucrose is the main photosynthesis product of plants and the fundamental carbon skeleton monomer and energy supply for seed formation and development. Drought stress induces decreased photosynthetic carbon assimilation capacity, and seriously affects seed weight in soybean. However, little is known about the relationship between decreases in soybean seed yield and disruption of sucrose metabolism and transport balance in leaves and seeds during the reproductive stages of crop growth. Three soybean cultivars with similar growth periods, “Shennong17”, “Shennong8”, and “Shennong12”, were subjected to drought stress during reproductive growth for 45 days. Drought stress significantly reduced leaf photosynthetic rate, shoot biomass, and seed weight by 63.93, 33.53, and 41.65%, respectively. Drought stress increased soluble sugar contents, the activities of sucrose phosphate synthase, sucrose synthase, and acid invertase enzymes, and up-regulated the expression levels of GmSPS1, GmSuSy2, and GmA-INV, but decreased starch content by 15.13% in leaves. Drought stress decreased the contents of starch, fructose, and glucose in seeds during the late seed filling stages, while it induced sucrose accumulation, which resulted in a decreased hexose-to-sucrose ratio. In developing seeds, the activities of sucrose synthesis and degradation enzymes, the expression levels of genes related to metabolism, and the expression levels of sucrose transporter genes were enhanced during early seed development under drought stress; however, under prolonged drought stress, all of them decreased. These results demonstrated that drought stress enhances the capacity for unloading sucrose into seeds and activated sucrose metabolism during early seed development. At the middle and late seed filling stages, sucrose flow from leaves to seeds was diminished, and the balance of sucrose metabolism was impaired in seeds, resulting in seed mass reduction. The different regulation strategies in sucrose allocation, metabolism, and transport during different seed development stages may be one of the physiological mechanisms for soybean plants to resist drought stress.

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“…Heterologous expression of ShINH1 confirmed its possible function as an invertase inhibitor [48]. In the same way, an apoplastic invertase inhibitor was shown to affect seed mass in soybean by regulating extracellular invertase during seed maturation [49]. Invertase inhibitor ZM-INVINH1 has been reported to bind cell wall invertase during grain development in maize [50].…”

Section: Discussionmentioning

confidence: 74%

Cell Wall Proteome of Wheat Grain Endosperm and Outer Layers at Two Key Stages of Early Development

Cherkaoui

Lollier

Geairon

et al. 2019

IJMS

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The cell wall is an important compartment in grain cells that fulfills both structural and functional roles. It has a dynamic structure that is constantly modified during development and in response to biotic and abiotic stresses. Non-structural cell wall proteins (CWPs) are key players in the remodeling of the cell wall during events that punctuate the plant life. Here, a subcellular and quantitative proteomic approach was carried out to identify CWPs possibly involved in changes in cell wall metabolism at two key stages of wheat grain development: the end of the cellularization step and the beginning of storage accumulation. Endosperm and outer layers of wheat grain were analyzed separately as they have different origins (maternal and seed) and functions in grains. Altogether, 734 proteins with predicted signal peptides were identified (CWPs). Functional annotation of CWPs pointed out a large number of proteins potentially involved in cell wall polysaccharide remodeling. In the grain outer layers, numerous proteins involved in cutin formation or lignin polymerization were found, while an unexpected abundance of proteins annotated as plant invertase/pectin methyl esterase inhibitors were identified in the endosperm. In addition, numerous CWPs were accumulating in the endosperm at the grain filling stage, thus revealing strong metabolic activities in the cell wall during endosperm cell differentiation, while protein accumulation was more intense at the earlier stage of development in outer layers. Altogether, our work gives important information on cell wall metabolism during early grain development in both parts of the grain, namely the endosperm and outer layers. The wheat cell wall proteome is the largest cell wall proteome of a monocot species found so far.

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Suppression of extracellular invertase inhibitor gene expression improves seed weight in soybean (Glycine max)

Abstract: HighlightThe roles of GmCIF1 and GmC/VIF1 as invertase inhibitors were examined in vitro in soybean (Glycine max), and post-translational elevation of extracellular invertase activity by silencing GmCIF1 expression was found to increase seed weight.

Cited by 52 publications

References 68 publications

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

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

Effect of Drought Stress during Soybean R2–R6 Growth Stages on Sucrose Metabolism in Leaf and Seed

Cell Wall Proteome of Wheat Grain Endosperm and Outer Layers at Two Key Stages of Early Development

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