Auxin controls Arabidopsis anther dehiscence by regulating endothecium lignification and jasmonic acid biosynthesis

Abstract

SUMMARYIt has been suggested that, in Arabidopsis, auxin controls the timing of anther dehiscence, possibly by preventing premature endothecium lignification. We show here that auxin content in anthers peaks before the beginning of dehiscence and decreases when endothecium lignification occurs. We show that, in the auxinperception mutants afb1-3 and tir1 afb2 afb3, endothecium lignification and anther dehiscence occur earlier than wild-type, and the gene encoding the transcription factor MYB26, which is required for endothecium lignification, is over-expressed specifically at early stages; in agreement, MYB26 expression is reduced in naphthalene acetic acid-treated anthers, and afb1 myb26 double mutants show no endothecial lignification, suggesting that auxin acts through MYB26. As jasmonic acid (JA) controls anther dehiscence, we analysed how auxin and JA interact. In the JA-defective opr3 mutant, indehiscent anthers show normal timing of endothecium lignification, suggesting that JA does not control this event. We show that expression of the OPR3 and DAD1 JA biosynthetic genes is enhanced in afb1-3 and tir1 afb2 afb3 flower buds, but is reduced in naphthalene acetic acid-treated flower buds, suggesting that auxin negatively regulates JA biosynthesis. The double mutant afb1 opr3 shows premature endothecium lignification, as in afb1-3, and indehiscent anthers due to lack of JA, which is required for stomium opening. By treating afb1 opr3 and opr3 inflorescences with JA, we show that a high JA content and precocious endothecium lignification both contribute to induction of early anther dehiscence. We propose that auxin controls anther dehiscence timing by negatively regulating two key events: endothecium lignification via MYB26, and stomium opening via the control of JA biosynthesis.

Jasmonoyl-l-Isoleucine Coordinates Metabolic Networks Required for Anthesis and Floral Attractant Emission in Wild Tobacco (Nicotiana attenuata)

“…Comparable roles for COI1 homologs in many other model plants have been confirmed (Li et al, 2004;Wang et al, 2005;Paschold et al, 2007;Ye et al, 2012). In several cases, such as the dehiscence of anthers or the growth of petals of Arabidopsis flowers, JA signaling has been shown to interact with other hormones such as auxins (Brioudes et al, 2009;Varaud et al, 2011;Cecchetti et al, 2013). In contrast with the JA-dependent regulation of male fecundity and petal growth in polypetalous plant species such as Arabidopsis, little is known about the role that JAs play in the timely development and opening process of functional petal complexes developed by sympetalous plants.…”

Transcription Factor MYB26 Is Key to Spatial Specificity in Anther Secondary Thickening Formation

“…Similar phenotypes to those seen with MYB26 are also generated by overexpression of the NST1 and NST2 genes (Mitsuda et al, 2005). Cecchetti et al (2013) demonstrated that the timing of anther dehiscence was negatively regulated by auxin inhibiting MYB26 expression and thus endothecium lignification, but also stomium opening via the control of jasmonic acid (JA) biosynthesis. It has recently been shown that an auxin maxima is formed due to transport of auxin from the tapetum into the middle cell layer, and this is important for the regulation of pollen development and dehiscence (Cecchetti et al, 2017).…”

Identification of metabolites involved in heat stress response in different tomato genotypes

“…In addition, mutations in auxin receptor encoding genes, such as transport inhibitor response 1 (tir1) and auxin signalling F box (afb) genes, resulted in early maturation of pollen due to pollen release before the filament was completely elongated (Cecchetti et al 2008, Cecchetti et al 2013. Cecchetti et al 2013 also proposed that auxin is involved in the coordination of pollen maturation and anther dehiscence. This is supported by the fact that expression of the indole acetic acid lysine synthetase (iaal) gene in anther tapetum of transgenic tobacco plants led to a decrease of auxin levels and a concomitant decrease in in vitro pollen embryogenesis (Yang et al 1997).…”

“…Blocking the auxin biosynthesis pathway in arabidopsis by various combinations of yuc loss-of-function mutants led to severe alterations in floral organ development and a lack of pollen production (Cheng et al 2006). In addition, mutations in auxin receptor encoding genes, such as transport inhibitor response 1 (tir1) and auxin signalling F box (afb) genes, resulted in early maturation of pollen due to pollen release before the filament was completely elongated (Cecchetti et al 2008, Cecchetti et al 2013. Cecchetti et al 2013 also proposed that auxin is involved in the coordination of pollen maturation and anther dehiscence.…”

“…Required for pollen germination (Mattioli et al 2012) Glutathione Required for pollen germination (Zechmann et al 2011) Required for floral organ development and pollen (Cheng et al 2006) Arabidopsis Auxin production arabidopsis Required for pollen maturation and anther dehiscence (Cecchetti et al 2013) thaliana…”