Original contributionHydrogen peroxide-mediated catalase gene expression in response to wounding
Introduction
Catalase (E.C.1.11.1.6 H2O2H2O2 oxidoreductase; CAT) is an iron porphyrin enzyme that catalyzes the dismutation of H2O2:H2O2 to water and dioxygen. CAT, along with hydroperoxidases and superoxide dismutases, serves as an efficient scavenger of ROS, preventing cellular damage. In maize, three catalase isozymes have been identified and characterized in various tissues [1]. CAT-1, CAT-2, and CAT-3 are encoded by the three unlinked structural genes Cat1, Cat2, and Cat3. The developmental expression pattern of each CAT is unique and complex. CAT-1 is the only catalase expressed in mature pollen and the immature milky endosperm. CAT-1 is also expressed in scutella in the early stages of kernel development, with highest activity levels in the late stages of kernel development. Upon imbibition and germination, CAT-1 is initially the only CAT isozyme expressed in the scutellum, but, as the embryo grows, CAT-1 diminishes and CAT-2 becomes the predominant isozyme, reaching an activity peak at about 4 dpi. In addition to developmental regulation, CAT expression is also influenced by many environmental factors such as light [2], plant hormones [3], ozone [4], temperature [5], xenobiotics [6], and hydrogen peroxide [7], underscoring the important protective roles of catalase in response to oxidative stress.
Environmental stress due to wounding greatly affects crop production. Plants respond quickly to wounding stress, such as physical injury and insect attack, by activating diverse genes that encode proteins involved in healing injured tissues. Some representative examples are the proteinase inhibitor genes, such as Pin2, that are transcriptionally activated by wounding [8]. A rapid increase in endogenous levels of ABA and JA occurs after wounding [9], and inhibitors of JA biosynthesis also inhibit the wound-induced expression of the proteinase inhibitor genes [10]. JA is regarded as one of the endogenous wound-induced signals involved in the expression of defensive genes, such as those for proteinase inhibitors. Other wound-inducible signaling molecules, such as systemin, oligogalacturonide, and ABA, have been shown to cause increased levels of endogenous JA [11]. ABA-deficient plants do not accumulate Pin2 mRNA upon wounding, indicating that ABA is required to function upstream of JA in the wound-induced signaling cascade [9], [12].
The carotenoid-deficient vp mutants of maize have great potential for providing information concerning the regulation of gene expression in response to ABA in both embryos and vegetative tissues [13]. A group of vp maize mutants are deficient in ABA (e.g., vp5) [12]. Seedlings rescued from vp5 kernels contain much less ABA (< 20%) than do wild-type seedlings, and the ABA concentration does not increase in response to water deficit [14].
In this paper, we demonstrate that each Cat gene responds differently to wounding in embryos and in leaves. In an effort to clarify the roles of JA and ABA, if any, in the maize Cat gene response to wounding in vegetative organs, we also examined the regulation of Cat gene expression in wild-type and vp5leaves subjected to wounding. The results presented here show that each Cat gene (Cat1, Cat2, and Cat3) responds differently to wounding in vp5 leaves. There is no change in Cat2 transcript accumulation in response to wounding. In contrast, the Cat1 and Cat3 transcripts increased dramatically in response to wounding in both wild type (Vp5/-) and mutant(vp5/vp5) leaves, suggesting that Cat1 and Cat3 expression in response to wounding may not be related to changes in endogenous ABA levels in leaves. Application of JA to leaves did not significantly induce Cat gene expression. Thus, an ABA-independent and JA-independent mechanism might be involved in Cat1 and Cat3 transcript accumulation in response to wounding in vegetative tissues. We have found that production of H2O2 is elevated in response to wounding. Thus, ROS is a likely mediator for wounding induced Cat gene expression.
Section snippets
Plant materials
The maize lines M1A4 (Vp5/-) and W64A were used in these studies. The maize vp5 mutant contains lowered amounts of ABA, resulting in precocious germination on the ear. The vp kernels can be distinguished from wild-type kernels early in development based on endosperm and embryo color. The vp5 mutation in M1A4 interrupts ABA biosynthesis early in the biosynthetic pathway [15]. Homozygous recessive kernels (vp5/vp5) lack carotenoids, resulting in white endosperm and embryos, easily distinguished
Cat gene expression in response to wounding and JA in 28 dpp developing embryos
Immature embryos were used to examine the wounding effects resulting from the removal of embryonic axes on the expression of the Cat genes in maize. In previous studies, we observed that Cat1 transcript increased in response to such minor environmental changes as removing embryos from kernels, removing plants from soil, and soaking in water [3]. We speculate that such increases in Cat transcript accumulation may be caused by a wounding-related signal. In 28 dpp embryos, the axis is still
Discussion
We have examined the expression of the three maize Cat genes in response to wounding and JA, in W64A, Vp5 wild-type, and vp5 mutant leaves, as well as in W64A embryos. Our results show that the pattern of Cat gene responses to wounding and to JA is different between embryos and leaves. In immature embryos, all three Cat genes are upregulated by wounding and JA, whereas in leaves, only the Cat1 and Cat3 genes are upregulated by wounding. In addition, application of JA does not affect Cat gene
Acknowledgements
We thank Stephanie Ruzsa and Sheri Kernodle for expert technical assistance. Research was supported in part by grants from the National Science Foundation and the Environmental Protection Agency.
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