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

Abstract

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.

An Invertase Inhibitor from Maize Localizes to the Embryo Surrounding Region during Early Kernel Development

“…A second possibility is that vacuolar-targeted IVR2, present in the ESR, is mis-localized to the cell wall. IVR2 has been localized to the pedicel region by in situ analysis (Andersen et al, 2002), and we have demonstrated a strong in situ hybridization signal for IVR2 transcript in the ESR at 5 DAP (Y. Wang and N.J. Bate, unpublished data). A third possibility is that ZM-INVINH1 functions to inhibit an as yet uncharacterized apoplastic invertase (INCW).…”

“…Mutations in this gene result in miniature kernels (the mn1 mutation) and have a severely reduced endosperm (Cheng et al, 1996;Vilhar et al, 2002). Recently, the association of a IVR2, a soluble invertase expressed during early kernel development, with seed yield under conditions of limiting photosynthesis suggests that soluble invertases also play a significant role in providing hexose sugars to support cell division during the prestorage phase (Andersen et al, 2002), as has been previously suggested (Zinselmeier et al, 1999).…”

“…Mutations in this gene result in miniature kernels (the mn1 mutation) and have a severely reduced endosperm (Cheng et al, 1996;Vilhar et al, 2002). Recently, the association of a IVR2, a soluble invertase expressed during early kernel development, with seed yield under conditions of limiting photosynthesis suggests that soluble invertases also play a significant role in providing hexose sugars to support cell division during the prestorage phase (Andersen et al, 2002), as has been previously suggested (Zinselmeier et al, 1999).Invertases exhibit complex regulation at the transcriptional and posttranscriptional levels in response to developmental, environmental, and carbohydrate signals (Sturm, 1999). In addition, small (Ͻ20-kD) inhibitor proteins (INVINH) have been associated with invertase preparations in a number of dicot plant species (Pressey, 1994;Weil et al, 1994;Krausgrill et al, 1996Krausgrill et al, , 1998Greiner et al, 1998Greiner et al, , 2000 since their first biochemical characterization (Pressey, 1966;Jaynes and Nelson, 1971).…”

Evidence That High Activity of Vacuolar Invertase Is Required for Cotton Fiber and Arabidopsis Root Elongation through Osmotic Dependent and Independent Pathways, Respectively

“…Most notably, the multicellular nature of plant tissues makes it difficult to quantitatively evaluate the contribution of VIN in specific cell types. For example, decrease of VIN expression is associated with maize ovary abortion or reduction in its expansion (Andersen et al, 2002;McLaughlin and Boyer, 2004). The VIN gene Ivr2, however, is expressed in nucellus and vascular bundles of the pedicel deeply embedded within the pericarp (Andersen et al, 2002).…”

“…High VIN expression or activity has been observed in a range of expanding tissues, including maize (Zea mays) ovaries (Andersen et al, 2002;McLaughlin and Boyer, 2004), grape (Vitis vinifera) berry (Davies and Robinson, 1996), carrot (Daucus carota) taproot (Tang et al, 1999), and sugar beet (Beta vulgaris) petioles (González et al, 2005). It is hypothesized that VIN may play a major role in plant cell expansion, a key step in plant cell development (González et al, 2005).…”