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NADPH Oxidase-Dependent Superoxide Production in Plant Reproductive Tissues.

Jiménez-Quesada MJ, Traverso JÁ, Alché Jde D - Front Plant Sci (2016)

Bottom Line: Respiratory burst oxidase homologs (Rbohs) are superoxide-producing enzymes involved in a broad range of processes in plant physiology.Rboh isoforms have been identified in both the male and female gametophyte and have proven to be tightly regulated.Their role at crucial points such as proper growth of pollen tube, self-incompatibility response and eventual fertilization is discussed.

View Article: PubMed Central - PubMed

Affiliation: Plant Reproductive Biology Laboratory, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental del Zaidín, Spanish National Research Council (CSIC) Granada, Spain.

ABSTRACT
In the life cycle of a flowering plant, the male gametophyte (pollen grain) produced in the anther reaches the stigmatic surface and initiates the pollen-pistil interaction, an important step in plant reproduction, which ultimately leads to the delivery of two sperm cells to the female gametophyte (embryo sac) inside the ovule. The pollen tube undergoes a strictly apical expansion characterized by a high growth rate, whose targeting should be tightly regulated. A continuous exchange of signals therefore takes place between the haploid pollen and diploid tissue of the pistil until fertilization. In compatible interactions, theses processes result in double fertilization to form a zygote (2n) and the triploid endosperm. Among the large number of signaling mechanisms involved, the redox network appears to be particularly important. Respiratory burst oxidase homologs (Rbohs) are superoxide-producing enzymes involved in a broad range of processes in plant physiology. In this study, we review the latest findings on understanding Rboh activity in sexual plant reproduction, with a particular focus on the male gametophyte from the anther development stages to the crowning point of fertilization. Rboh isoforms have been identified in both the male and female gametophyte and have proven to be tightly regulated. Their role at crucial points such as proper growth of pollen tube, self-incompatibility response and eventual fertilization is discussed.

No MeSH data available.


Related in: MedlinePlus

Rboh-dependent superoxide production during gametophyte development. Location of  during the development of gametophytes. (A) Two selected stages of late anther development (tetrads and microspores) and anthers at the dehiscence stage. (B) Three selected female gametophyte development stages, including the pre-meiotic phase, functional megaspore formation and the fully developed embryo sac stage. The localization of H2O2 accumulation is also shown when necessary (for more detailed information, see text above). Recognized sources of superoxide are marked in black. Blue star: ; red star: H2O2; T, tetrads; M, microspore; Mp, mature pollen; Mmc, megaspore mother cell; Fm, functional megaspore; Dm, degenerating megaspore; Ac, antipodal cell; Cc, central cell; S, synergid; E, egg cell; Mi, micropyle.
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Figure 1: Rboh-dependent superoxide production during gametophyte development. Location of during the development of gametophytes. (A) Two selected stages of late anther development (tetrads and microspores) and anthers at the dehiscence stage. (B) Three selected female gametophyte development stages, including the pre-meiotic phase, functional megaspore formation and the fully developed embryo sac stage. The localization of H2O2 accumulation is also shown when necessary (for more detailed information, see text above). Recognized sources of superoxide are marked in black. Blue star: ; red star: H2O2; T, tetrads; M, microspore; Mp, mature pollen; Mmc, megaspore mother cell; Fm, functional megaspore; Dm, degenerating megaspore; Ac, antipodal cell; Cc, central cell; S, synergid; E, egg cell; Mi, micropyle.

Mentions: In angiosperms, the female gametophyte or megagametophyte, is the embryo sac originating from a haploid megaspore. During gametogenesis, mitochondria have been established as the primary source of mainly superoxide and hydrogen peroxide (Martin et al., 2014a). Although ROS have been shown to be not just involved in but also tightly regulated in megagametogenesis (Martin et al., 2013, 2014b), little information on ROS/superoxide during female gametophyte development is available. These studies analyze female gametophytic mutants impaired in MnSOD activity which show infertility caused by various defects ranging from development arrest to aberrant egg apparatus. In WT ovules, ROS (H2O2) were detected early on in the process, when megaspore cell death takes place (Figure 1B). At a later stage of development, the mature female gametophyte showed both mitochondrial superoxide and peroxide accumulation in the central cell, whereas cytosolic superoxide was only detected outside the embryo sac at the micropylar portion (Figure 1B). Alternatively, as the mutant ovules showed abnormally high levels of ROS, including cytosolic superoxide, the authors suggest that other sources of ROS, such as NADPH oxidase, might also be involved. Transcriptome data concerning ovule development have demonstrated that RbohD shows the highest expression, whereas other Rboh isoforms display quite low expression levels (Wynn et al., 2011). To our knowledge, no female gametophyte-specific Rbohs have been described to date.


NADPH Oxidase-Dependent Superoxide Production in Plant Reproductive Tissues.

Jiménez-Quesada MJ, Traverso JÁ, Alché Jde D - Front Plant Sci (2016)

Rboh-dependent superoxide production during gametophyte development. Location of  during the development of gametophytes. (A) Two selected stages of late anther development (tetrads and microspores) and anthers at the dehiscence stage. (B) Three selected female gametophyte development stages, including the pre-meiotic phase, functional megaspore formation and the fully developed embryo sac stage. The localization of H2O2 accumulation is also shown when necessary (for more detailed information, see text above). Recognized sources of superoxide are marked in black. Blue star: ; red star: H2O2; T, tetrads; M, microspore; Mp, mature pollen; Mmc, megaspore mother cell; Fm, functional megaspore; Dm, degenerating megaspore; Ac, antipodal cell; Cc, central cell; S, synergid; E, egg cell; Mi, micropyle.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4815025&req=5

Figure 1: Rboh-dependent superoxide production during gametophyte development. Location of during the development of gametophytes. (A) Two selected stages of late anther development (tetrads and microspores) and anthers at the dehiscence stage. (B) Three selected female gametophyte development stages, including the pre-meiotic phase, functional megaspore formation and the fully developed embryo sac stage. The localization of H2O2 accumulation is also shown when necessary (for more detailed information, see text above). Recognized sources of superoxide are marked in black. Blue star: ; red star: H2O2; T, tetrads; M, microspore; Mp, mature pollen; Mmc, megaspore mother cell; Fm, functional megaspore; Dm, degenerating megaspore; Ac, antipodal cell; Cc, central cell; S, synergid; E, egg cell; Mi, micropyle.
Mentions: In angiosperms, the female gametophyte or megagametophyte, is the embryo sac originating from a haploid megaspore. During gametogenesis, mitochondria have been established as the primary source of mainly superoxide and hydrogen peroxide (Martin et al., 2014a). Although ROS have been shown to be not just involved in but also tightly regulated in megagametogenesis (Martin et al., 2013, 2014b), little information on ROS/superoxide during female gametophyte development is available. These studies analyze female gametophytic mutants impaired in MnSOD activity which show infertility caused by various defects ranging from development arrest to aberrant egg apparatus. In WT ovules, ROS (H2O2) were detected early on in the process, when megaspore cell death takes place (Figure 1B). At a later stage of development, the mature female gametophyte showed both mitochondrial superoxide and peroxide accumulation in the central cell, whereas cytosolic superoxide was only detected outside the embryo sac at the micropylar portion (Figure 1B). Alternatively, as the mutant ovules showed abnormally high levels of ROS, including cytosolic superoxide, the authors suggest that other sources of ROS, such as NADPH oxidase, might also be involved. Transcriptome data concerning ovule development have demonstrated that RbohD shows the highest expression, whereas other Rboh isoforms display quite low expression levels (Wynn et al., 2011). To our knowledge, no female gametophyte-specific Rbohs have been described to date.

Bottom Line: Respiratory burst oxidase homologs (Rbohs) are superoxide-producing enzymes involved in a broad range of processes in plant physiology.Rboh isoforms have been identified in both the male and female gametophyte and have proven to be tightly regulated.Their role at crucial points such as proper growth of pollen tube, self-incompatibility response and eventual fertilization is discussed.

View Article: PubMed Central - PubMed

Affiliation: Plant Reproductive Biology Laboratory, Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental del Zaidín, Spanish National Research Council (CSIC) Granada, Spain.

ABSTRACT
In the life cycle of a flowering plant, the male gametophyte (pollen grain) produced in the anther reaches the stigmatic surface and initiates the pollen-pistil interaction, an important step in plant reproduction, which ultimately leads to the delivery of two sperm cells to the female gametophyte (embryo sac) inside the ovule. The pollen tube undergoes a strictly apical expansion characterized by a high growth rate, whose targeting should be tightly regulated. A continuous exchange of signals therefore takes place between the haploid pollen and diploid tissue of the pistil until fertilization. In compatible interactions, theses processes result in double fertilization to form a zygote (2n) and the triploid endosperm. Among the large number of signaling mechanisms involved, the redox network appears to be particularly important. Respiratory burst oxidase homologs (Rbohs) are superoxide-producing enzymes involved in a broad range of processes in plant physiology. In this study, we review the latest findings on understanding Rboh activity in sexual plant reproduction, with a particular focus on the male gametophyte from the anther development stages to the crowning point of fertilization. Rboh isoforms have been identified in both the male and female gametophyte and have proven to be tightly regulated. Their role at crucial points such as proper growth of pollen tube, self-incompatibility response and eventual fertilization is discussed.

No MeSH data available.


Related in: MedlinePlus