A Re-Evaluation of the Relative Roles of Two Invertases, INCW2 and IVR1, in Developing Maize Kernels and Other Tissues

Carlson, Susan; Chourey, Prem S.

doi:10.1104/pp.121.3.1025

Cited by 31 publications

(29 citation statements)

References 38 publications

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“…The cell wall-bound invertase in the cell wall space can facilitate assimilate transfer from maternal tissues to the developing endosperm because lack of symplastic connections between these tissues necessitates an apoplastic cell wall step (Felker and Shannon, 1980). This is consistent with the suggestion that Incw2 is expressed primarily in filial cells (Carlson and Chourey, 1999). However, during early phases of growth, the kernel is almost entirely maternal tissue.…”

Section: Soluble Invertase and Hexose To Suc Balance In Young Ovariessupporting

confidence: 79%

“…7), together with contrasting developmental profiles for Ivr2 and Incw2 mRNA (Fig. 6), clearly support distinct temporal roles that were not readily resolvable by concurrent extraction of both enzymes in more mature kernels (Carlson and Chourey, 1999). The role of the Incw2 cell wall-bound invertase activity in Suc hydrolysis and assimilate transfer to developing endosperm at a later stage of kernel development has been detailed previously (Cheng et al, 1996).…”

Section: Soluble Invertase and Hexose To Suc Balance In Young Ovariesmentioning

confidence: 86%

“…Commuri, K.E. Koch, and R.J. Jones, unpublished data), with little or no detection of either Ivr1 or Ivr2 transcripts later in kernel development Carlson and Chourey, 1999; P.D. Coummuri, K.E.…”

Section: Invertase Mrna Levels and Activitymentioning

confidence: 99%

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Soluble Invertase Expression Is an Early Target of Drought Stress during the Critical, Abortion-Sensitive Phase of Young Ovary Development in Maize

et al. 2002

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To distinguish their roles in early kernel development and stress, expression of soluble (Ivr2) and insoluble (Incw2) acid invertases was analyzed in young ovaries of maize (Zea mays) from 6 d before (Ϫ6 d) to 7 d after pollination (ϩ7 d) and in response to perturbation by drought stress treatments. The Ivr2 soluble invertase mRNA was more abundant than the Incw2 mRNA throughout pre-and early post-pollination development (peaking at ϩ3 d). In contrast, Incw2 mRNAs increased only after pollination. Drought repression of the Ivr2 soluble invertase also preceded changes in Incw2, with soluble activity responding before pollination (Ϫ4 d). Distinct profiles of Ivr2 and Incw2 mRNAs correlated with respective enzyme activities and indicated separate roles for these invertases during ovary development and stress. In addition, the drought-induced decrease and developmental changes of ovary hexose to sucrose ratio correlated with activity of soluble but not insoluble invertase. Ovary abscisic acid levels were increased by severe drought only at Ϫ6 d and did not appear to directly affect Ivr2 expression. In situ analysis showed localized activity and Ivr2 mRNA for soluble invertase at sites of phloem-unloading and expanding maternal tissues (greatest in terminal vascular zones and nearby cells of pericarp, pedicel, and basal nucellus). This early pattern of maternal invertase localization is clearly distinct from the well-characterized association of insoluble invertase with the basal endosperm later in development. This localization, the shifts in endogenous hexose to sucrose environment, and the distinct timing of soluble and insoluble invertase expression during development and stress collectively indicate a key role and critical sensitivity of the Ivr2 soluble invertase gene during the early, abortion-susceptible phase of development.

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Section: Soluble Invertase and Hexose To Suc Balance In Young Ovariessupporting

confidence: 79%

Section: Soluble Invertase and Hexose To Suc Balance In Young Ovariesmentioning

confidence: 86%

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Soluble Invertase Expression Is an Early Target of Drought Stress during the Critical, Abortion-Sensitive Phase of Young Ovary Development in Maize

et al. 2002

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“…Xu et al (1996) reported abundant levels of the two soluble invertases, Ivr1 and Ivr2, in developing kernels. However, subsequent analyses (Carlson and Chourey 1999;Anderson et al 2002;McLaughlin and Boyer 2004) report no Ivr1 expression in this tissue and the Ivr2 expression is predominantly localized in the maternal tissues, nucellus and pedicel, and is temporally restricted to the very early stages (up to the 8 DAP stage) of kernel development. A similar tissue profile of soluble invertase is also described in developing caryopsis of barley (Weschke et al 2003).…”

Section: Introductionmentioning

confidence: 93%

Genetic control of cell wall invertases in developing endosperm of maize

Chourey

Jain

et al. 2005

Planta

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We show here that the total invertase activity in developing seeds of maize is due to two cell wall invertase (CWI) genes, Incw1 and Incw2 (Mn1). Our previous results have shown that loss-of-function mutations at the Mn1 locus lead to the miniature-1 (mn1) seed phenotype, marked by a loss of >70% of seed weight at maturity. The mn1 seed mutant is, however, non-lethal presumably because it retains a residual low level, approximately 1%, of the total CWI activity relative to the Mn1 endosperm throughout seed development. Evidence here shows that the residual activity in the mn1 mutant is encoded by the Incw1 gene. RNA level analyses, especially quantitative real-time PCR studies, showed significant spatial and temporal heterogeneity in the expression of the two CWI genes in the developing endosperm. The Mn1-encoded Incw2 transcripts were seen at the highest levels in the basal region (the sugar unloading zone) during the early phase of cell division and elongation in the endosperm. In contrast, the highest levels of Incw1 transcripts were seen in the storage phase in both the upper (storage cells) and the lower parts of the endosperm. Protein and enzyme level analyses, however, appeared to show a lack of concordance with the RNA level of expression in both the Mn1 and mn1 endosperms, indicating a possibility of post-transcriptional control in the expression of these two genes. Collectively, the data suggest an important role for apoplastic cleavage of sucrose throughout the duration of seed development; and, of the two isoforms, the INCW2 appears to control metabolic flux of sugar utilization in the developing endosperm.

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“…Thereafter, the membranes were blocked with 5% nonfat dry milk in PBS, pH 7.2, plus 0.1% Tween 20 and then probed for either cell wall invertase using polyclonal anti-maize INCW2 antibodies raised in mice (Carlson and Chourey, 1999) or for INVINH1 using antibodies raised in rabbit against a synthetic peptide of NNNLVETTC derived from the N terminus of INVINH1 (Mimotopes). Protein signals were detected using goat anti-mouse or anti-rabbit IgG conjugated with horseradish peroxidize for cell wall invertase and INVINH1, respectively, followed by visualization using a chemiluminescence system and densitometric quantification using the Image J program (http://rsb.info.nih.gov/ij/).…”

Section: Protein Gel Blot Analysesmentioning

confidence: 99%

Posttranslational Elevation of Cell Wall Invertase Activity by Silencing Its Inhibitor in Tomato Delays Leaf Senescence and Increases Seed Weight and Fruit Hexose Level

2009

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Invertase plays multiple pivotal roles in plant development. Thus, its activity must be tightly regulated in vivo. Emerging evidence suggests that a group of small proteins that inhibit invertase activity in vitro appears to exist in a wide variety of plants. However, little is known regarding their roles in planta. Here, we examined the function of INVINH1, a putative invertase inhibitor, in tomato (Solanum lycopersicum). Expression of a INVINH1:green fluorescent protein fusion revealed its apoplasmic localization. Ectopic overexpression of INVINH1 in Arabidopsis thaliana specifically reduced cell wall invertase activity. By contrast, silencing its expression in tomato significantly increased the activity of cell wall invertase without altering activities of cytoplasmic and vacuolar invertases. Elevation of cell wall invertase activity in RNA interference transgenic tomato led to (1) a prolonged leaf life span involving in a blockage of abscisic acid-induced senescence and (2) an increase in seed weight and fruit hexose level, which is likely achieved through enhanced sucrose hydrolysis in the apoplasm of the fruit vasculature. This assertion is based on (1) coexpression of INVINH1 and a fruit-specific cell wall invertase Lin5 in phloem parenchyma cells of young fruit, including the placenta regions connecting developing seeds; (2) a physical interaction between INVINH1 and Lin5 in vivo; and (3) a symplasmic discontinuity at the interface between placenta and seeds. Together, the results demonstrate that INVINH1 encodes a protein that specifically inhibits the activity of cell wall invertase and regulates leaf senescence and seed and fruit development in tomato by limiting the invertase activity in planta.

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A Re-Evaluation of the Relative Roles of Two Invertases, INCW2 and IVR1, in Developing Maize Kernels and Other Tissues

Cited by 31 publications

References 38 publications

Soluble Invertase Expression Is an Early Target of Drought Stress during the Critical, Abortion-Sensitive Phase of Young Ovary Development in Maize

Soluble Invertase Expression Is an Early Target of Drought Stress during the Critical, Abortion-Sensitive Phase of Young Ovary Development in Maize

Genetic control of cell wall invertases in developing endosperm of maize

Posttranslational Elevation of Cell Wall Invertase Activity by Silencing Its Inhibitor in Tomato Delays Leaf Senescence and Increases Seed Weight and Fruit Hexose Level

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