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

Abstract

Life in unpredictably changing habitats is a great challenge, especially for sessile organisms like plants. Fruit and seed heteromorphism is one way to cope with such variable environmental conditions. It denotes the production of distinct types of fruits and seeds that often mediate distinct life-history strategies in terms of dispersal, germination and seedling establishment. But although the phenomenon can be found in numerous species and apparently evolved several times independently, its developmental time course or molecular regulation remains largely unknown. Here, we studied fruit development in Aethionema arabicum, a dimorphic member of the Brassicaceae family. We characterized fruit morph differentiation by comparatively analyzing discriminating characters like fruit growth, seed abortion and dehiscence zone development. Our data demonstrate that fruit morph determination is a 'last-minute' decision happening in flowers after anthesis directly before the first morphotypical differences start to occur. Several growth experiments in combination with hormone and gene expression analyses further indicate that an accumulation balance of the plant hormones auxin and cytokinin in open flowers together with the transcript abundance of the Ae. arabicum ortholog of BRANCHED1, encoding a transcription factor known for its conserved function as a branching repressor, may guide fruit morph determination. Thus, we hypothesize that the plasticity of the fruit morph ratio in Ae. arabicum may have evolved through the modification of a preexisting network known to govern correlative dominance between shoot organs.

Fracture of the dimorphic fruits ofAethionema arabicum(Brassicaceae)

“…The presented anatomical observations across a range of hierarchical levels contribute to our understanding of dimorphic structures and functions, and further support our knowledge of how these interact as bet-hedging adaptations to the physical environment. Together with recently published (Lenser et al 2018;Wilhelmsson et al 2019) and future molecular work into the mechanisms of the diaspore dimorphism in A. arabicum, the integration of biomechanics and imaging makes it an exciting time to study fruit-and dispersal-related properties by moving beyond Arabidopsis and other monomorphic plants.…”

“…Indeed, in A. arabicum, expression analyses in mature fruit have previously revealed that the orthologue IND (which is involved in the differentiation of the separation layer and acts as the key regulator in controlling valve margin specification) was down-regulated in IND fruit compared with DEH fruit (Lenser et al 2016). The genetic pathways operating in DEH and IND fruit therefore indicate an avenue for more detailed developmental and molecular time-course characterisations in A. arabicum, particularly with reference to valve-margin-specific and dehiscence zone identity genes (Avino et al 2012;Lenser et al 2018).…”

“…In comparison, the more dormant IND fruit abscises from the mother plant in its entirety, and has the capacity to disperse longer distances (telechory) via wind and water . The production of no intermediate morphs, together with a published genome sequence (Haudry et al 2013), contributes to the suitability of A. arabicum as an excellent model system for fruit and seed dimorphism (Lenser et al 2018;Mohammadin et al 2018;Arshad et al 2019;Wilhelmsson et al 2019).…”

Dispersal biophysics and adaptive significance of dimorphic diaspores in the annual Aethionema arabicum (Brassicaceae)

“…An advantage of A. arabicum as a model system for diaspore heteromorphism is that it exhibits true seed and fruit dimorphism with no intermediate morphs. Two distinct fruit types are produced on the same fruiting inflorescence (infructescence): dehiscent (DEH) fruits with four to six mucilaginous (M + ) seeds, and indehiscent (IND) fruits each containing a single nonmucilaginous (M − ) seed (Lenser et al ., , ). Upon maturity, dehiscence of the DEH fruit morph leads to the dispersal of M + seeds, while the IND fruit morph is dispersed in its entirety by abscission.…”

Seed Heteromorphism: An Important Adaptation of Halophytes for Habitat Heterogeneity

“…Up to now, many published papers have been focused in characterizing the germination pattern and dormancy mechanism in heteromorphic seeds of halophytes, especially in Amaranthaceae. Recently, it has been shown in a non-halophytic plant species- Aethionema arabicum that seed dimorphism was associated with several physiological and anatomical features and gene expression levels between the fruit and seed morphs ( Lenser et al, 2016 ) and latter it was found that cytokinin, and transcripts of BRANCHED1 gene were involved in governing fruit dimorphism ( Lenser et al, 2018 ). In this brief review, germination pattern of different dimorphs and factors which influence seed germination of those dimorphs have been discussed.…”