Jasmonate Signaling during Arabidopsis Stamen Maturation

Abstract

The last stages of stamen development, collectively called stamen maturation, encompass pollen viability, filament elongation and anther dehiscence or opening. These processes are essential for male fertility in Arabidopsis and require the function of jasmonate signaling. There is a good understanding of jasmonate synthesis, perception and transcriptional outputs in Arabidopsis stamens. In addition, the spatiotemporal localization of jasmonate signaling components at the tissue and cellular levels has started to emerge in recent years. However, the ultimate cellular functions activated by jasmonate to promote stamen maturation remain unknown. The hormones auxin and gibberellin have been proposed to control the activation of jasmonate synthesis to promote stamen maturation, although we hypothesize that this action is rather indirect. In this review, we examine these different areas, attempt to clarify some confusing aspects found in the literature and raise testable hypothesis that may help to further understand how jasmonate controls male fertility in Arabidopsis.

Keywords: Anther dehiscence; Auxin; Filament elongation; Jasmonate; Pollen viability; Stamen maturation.

Fig. 1

Jasmonate signaling during Arabidopsis stamen maturation. See main text for details. (A) Filament (F) elongation starts in wild-type (WT) Arabidopsis stamens at flower stage 12, and it finishes at stage 13 along with anther (A) opening. These processes fail in the jasmonate synthesis mutant aos. Notice that two of the six stamens in Arabidopsis flowers are always shorter and delayed. (B) Jasmonate synthesis pathway in stamens. The genes encoding the corresponding enzymes at each step are abbreviated in bold and italics. Question marks indicate that it is not yet clear which specific AOC and JAR1-type enzymes are required in stamens. 13-HPOT, 13(S)-hydroperoxy-octadecatrienoic acid; 12,13-EOT, (13S)-12,13-epoxy-octadecatrienoic acid.

Fig. 2

Proposed mechanism of jasmonate perception and transcriptional control of jasmonate-responsive genes with factors known to work during Arabidopsis stamen maturation. See main text for details.

Fig. 3

Schematic representation of Arabidopsis anther cross-sections at stages 11 and 12. Distinct cell types are shown with different colors. The tapetum layer is not visible anymore at stage 12. Red bars on the endothecium layer represent secondary thickenings. At stage 12 in this depiction, septum rupture is complete in both locule pairs, while stomium breakage to allow pollen release has only occurred in the right locule pair.

Fig. 4

Interaction model of jasmonate with auxin and gibberellin during stamen maturation. We propose that gibberellin (GA) and auxin allow normal filament development, which is required to activate jasmonate (JA) synthesis via DAD1. Moreover, gibberellin potentially promotes AGAMOUS function, which may also induce DAD1 expression. The low specific levels of auxin required to activate ARF6/8 function might be reached through catabolism with a DAO enzyme or through downregulation of the auxin synthesis genes YUCCA 2/6 mediated by a putative FTIP-like factor. ARF6/8 also contributes independently to anther opening by activating MYB26 expression. See main text for further details.