Thiol-based redox regulation in sexual plant reproduction: new insights and perspectives

Abstract

The success of sexual reproduction in plants involves (i) the proper formation of the plant gametophytes (pollen and embryo sac) containing the gametes, (ii) the accomplishment of specific interactions between pollen grains and the stigma, which subsequently lead to (iii) the fusion of the gametes and eventually to (iv) the seed setting. Owing to the lack of mobility, plants have developed specific regulatory mechanisms to control all developmental events underlying the sexual plant reproduction according to environmental challenges. Over the last decade, redox regulation and signaling have come into sight as crucial mechanisms able to manage critical stages during sexual plant reproduction. This regulation involves a complex redox network which includes reactive oxygen species (ROS), reactive nitrogen species (RNS), glutathione and other classic buffer molecules or antioxidant proteins, and some thiol/disulphide-containing proteins belonging to the thioredoxin superfamily, like glutaredoxins (GRXs) or thioredoxins (TRXs). These proteins participate as critical elements not only in the switch between the mitotic to the meiotic cycle but also at further developmental stages of microsporogenesis. They are also implicated in the regulation of pollen rejection as the result of self-incompatibility. In addition, they display precise space-temporal patterns of expression and are present in specific localizations like the stigmatic papillae or the mature pollen, although their functions and subcellular localizations are not clear yet. In this review we summarize insights and perspectives about the presence of thiol/disulphide-containing proteins in plant reproduction, taking into account the general context of the cell redox network.

Keywords: glutaredoxin; pistil; pollen; pollen-pistil interaction; redox regulation; sexual plant reproduction; stigma; thioredoxin.

Figure 1

ROS/NO are implicated in plant reproduction signaling. Model gynoecium of an Angiosperm. (A) Receptive stigma at high magnification, before pollen-pistil interaction. Pollen grains are active NO producers, while the receptive stigma papillae generate large quantities of H₂O₂ and display enhanced peroxidase activity, in some cases in the form of stigma-specific peroxidase (SSP). (B) Stigma and pollen grains during diverse phases of their interaction. Both the enhanced peroxidase activity and the high levels of H₂O₂ become significantly reduced after pollen landing on the stigma and pollen germination, likely through pollen-produced NO signaling. The germinating pollen grains and the elongating pollen tubes produce ROS and NO, particularly at their tips. (C) The embryo sac is reached by the pollen tube tip trough the micropylar end. NO produced in micropyle could be involved in pollen tube guidance.

Figure 2

Thiol-based redox proteins are critically involved in male gametogenesis, anther development and dehiscence. (A) Ontogenic development of the male germline. CC-type GRXs are essential for the switch from mitosis to meiosis in the microsporocytes (blue arrow), which ultimately originate the haploid pollen grains. They also participate in the development of the anther layers surrounding the microsporocytes (red arrows). (B) Diagram representing the histological structure of an anther (transversal section) and major changes occurring after dehiscence. H₂O₂ is required for cell wall lignification, which induces a thickening of the endotecium leading to anther dehiscence. CBSXs can regulate the level of H₂O₂ via their ability to active TRXs, which ultimately reduce PRXs in the plastids. This activity is enhanced by the presence of AMP, thus connecting the nutrition state with anther development.

Figure 3

Redoxins and related proteins are critical for pollen-pistil interactions. Illustration of the stigma and style during pollen-pistil interaction. (A) Representation of a pollen grain and the pollen coat. The presence of redoxins has been described both within the pollen grain and in the pollen coat. It is particularly remarkable the specific and conserved occurrence of h-type TRXs in the pollen grains, which can be secreted to the pollen coat. We hypothesize that N-terminal lipidations may play a role in this mechanism of secretion. Also, some redoxins synthesized in the tapetum may become integrated into the pollen coat after tapetum degeneration (B) Image representing the initial stages of the pollen-stigma interaction. Upon pollen arrival, pollen starts to hydrate, rapidly releasing GRXs present in the pollen coat. Also, the stigmatic papillae are rich in subgroup 1 TRXs. These TRXs have been involved in SI processes in Brassica although their occurrence has also been described for self-compatible species. (C) Representation of a pollen tube growing throughout the transmitting tissues of the style. Different types of redoxins are present in the pollen tube, some of them being secreted to the extracellular matrix of the transmitting tissue. Other redoxins are mainly expressed in stylar cells and may also be secreted to the extracellular matrix. Several redoxins related to photosynthesis are specifically expressed in the cells of the stylar tissues, which suggest that high photosynthetic rates are probably supporting pollen tube growth.