An INDEHISCENT-Controlled Auxin Response Specifies the Separation Layer in Early Arabidopsis Fruit

Abstract

Seed dispersal is an important moment in the life cycle of a plant species. In Arabidopsis thaliana, it is dependent on transcription factor INDEHISCENT (IND)-mediated specification of a separation layer in the dehiscence zone found in the margin between the valves (carpel walls) and the central replum of the developing fruit. It was proposed that IND specifies the separation layer by inducing a local auxin minimum at late stages of fruit development. Here we show that morphological differences between the ind mutant and wild-type fruit already arise at early stages of fruit development, coinciding with strong IND expression in the valve margin. We show that IND-reduced PIN-FORMED3 (PIN3) auxin efflux carrier abundance leads to an increased auxin response in the valve margin during early fruit development, and that the concomitant cell divisions that form the dehiscence zone are lacking in ind mutant fruit. Moreover, IND promoter-driven ectopic expression of the AGC kinases PINOID (PID) and WAG2 induced indehiscence by expelling auxin from the valve margin at stages 14-16 of fruit development through increased PIN3 abundance. Our results show that IND, besides its role at late stages of Arabidopsis fruit development, functions at early stages to facilitate the auxin-triggered cell divisions that form the dehiscence zone.

When the BRANCHED network bears fruit: how carpic dominance causes fruit dimorphism in Aethionema

“…A recent study in A . thaliana showed that cell differentiation related to dehiscence zone formation is initiated in open flowers after pollination (van Gelderen et al ., ), which closely corresponds to the developmental stage where first signs of dehiscence zone differentiation were also detected in the dehiscent morph of Ae . arabicum (Figures and S2).…”

Auxin Is Required for Valve Margin Patterning in Arabidopsis After All

“…In this new study (van Gelderen et al, 2016), the authors first confirmed that dehiscence zone formation does take place at the early fruit stages 14-16, as previously reported (Wu et al, 2006). As expected, no cell division or differentiation events occurred in this region in the shatter-resistant ind-2 mutant, also in line with previous findings (Liljegren et al, 2004).…”

“…In stage 17B, the authors confirm that also with the DR5 reporter an auxin minimum is present at the separation layer (van Gelderen et al, 2016), as previously reported (Sorefan et al, 2009). In the ind-2 mutant fruits, based on analysis with the DR5 reporter, the auxin response around the valve margins was low from stage 13-17A, and at stage 17B a sudden increase of auxin response in the replum was observed (van Gelderen et al, 2016).…”

“…Although, based on the DII, increased auxin should be present in the valve margin from stage 14, this could not be visualized with the DR5 reporter, but an increase in auxin response visualized with the DR5 reporter was observed from stage 15-17A. In stage 17B, the authors confirm that also with the DR5 reporter an auxin minimum is present at the separation layer (van Gelderen et al, 2016), as previously reported (Sorefan et al, 2009). In the ind-2 mutant fruits, based on analysis with the DR5 reporter, the auxin response around the valve margins was low from stage 13-17A, and at stage 17B a sudden increase of auxin response in the replum was observed (van Gelderen et al, 2016).…”

“…The DR5 reporter line transcriptionally responds to auxin and the DII reporter line works in the opposite sense, as DII:YFP gets degraded in the presence of auxin, and when comparing with the stable auxin-resistant mDII control reporter line, it allows for semiquantitative measurements of auxin input. Based on the DII reporter line, at stage 13, during pollination, auxin was low in the valve, valve margin, and replum (van Gelderen et al, 2016). The mDII signal remained constant from stage 13-17A, but from stages 14-17A the DII signal gradually decreased in the valve margin, coinciding with a strong decrease in the replum and carpels, suggesting that the auxin response increased from stage 14-17A.…”