MPF2-Like-A MADS-Box Genes Control the Inflated Calyx Syndrome in Withania (Solanaceae): Roles of Darwinian Selection

Abstract

The Chinese lantern, which is the inflated calyx syndrome (ICS) of Physalis, is formed by MPF2 in the presence of the plant hormones, cytokinin and gibberellin. MPF2 knockdown mutants of Physalis have small leaves, no ICS, and are male sterile, thus, revealing three MPF2-related functions. Of the close relatives of Physalis, Tubocapsicum has only a rudimentary calyx, whereas others, like the Withania species, have ICS. From all Withania samples tested, two classes of MPF2-like orthologs, MPF2-like-A and MPF2-like-B, were isolated, whereas only the latter class was obtained from tetraploid Tubocapsicum. Though distinct differences can be observed between MPF2-like-A and MPF2-like-B proteins, that is MPF2-like-A proteins have an aberrant structure in that they have a three amino acid deletion in their C-domain and an eight amino acid extension at the C-terminal end, MPF2-like-A genes are phylogenetically closer to the Physalis MPF2-like genes. Unlike MPF2-like-B, the overexpression of MPF2-like-A in Arabidopsis revealed extra large sepals thus suggesting that MPF2-like-A genes are very likely responsible for the ICS formation in Withania. This correlated with the expression pattern of MPF2-like-A in vegetative and flower tissues, whereas MPF2-like-B is expressed only in vegetative tissues of Withania. In Tubocapsicum, however, MPF2-like-B RNA is detectable in all tissues tested. Finally, positive Darwinian selection was observed in the branch leading to Physalis MPF2-like and Withania MPF2-like-A proteins, followed by purifying selection once the trait had evolved. By contrast, purifying selection was detected for all other MPF2-like proteins tested. The contribution of the MPF2-like gene duplication to subfunctionalization is discussed.

Plant hormones including ethylene are recruited in calyx inflation in Solanaceous plants

“…All together 13 accessions of Withania, including 5 species (W. aristata, W. frutescens, W. riebeckii, W. coagulans and W. somnifera) and 2 accessions of Tubocapsicum anomalum and one accession each for Iochroma australe, Vassobia breviflora and Physalis peruviana, were used for this study (see Khan et al, 2009). All of the accessions were grown in glasshouses of the Max-Planck-Institute for Plant Breeding Research (MPIPZ), Cologne, as described in Khan et al (2009).…”

“…All of the accessions were grown in glasshouses of the Max-Planck-Institute for Plant Breeding Research (MPIPZ), Cologne, as described in Khan et al (2009).…”

“…However, Solanum and Physalis are distant relatives and may not provide the appropriate material for comparative study of hormonal and molecular interactions. Interestingly, Withania and Tubocapsicum, which are closely related to Physalis and sisters to each other, may offer the most suitable materials for a comparative study (Khan et al, 2009). Withania exhibits a variety of inflated calyces, while Tubocapscium is an evolutionary natural loss mutant of the ICS.…”

Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies

“…MPF2, another member of the STMADS11 subfamily in Physalis floridana (Solanaceae), has been shown to control the inflated-calyx syndrome, which is a morphological novelty in which sepals resume growth after pollination in order to protect the mature fruit (He and Saedler, 2005;He and Saedler, 2007). Furthermore, gene duplication of MPF2-like genes followed by functional diversification at the regulatory and protein levels can be linked to the complex evolution of sepal morphologies in Solanaceae (Khan et al, 2009). …”

A novel phytoene synthase paralog from halophytic Salicorniaconfers salinity tolerance in plants

“…These fragments were recombined with pDONR 201 (Invitrogen) by BP recombination and later with destination vector pXCSG-mYFP (Feys et al, 2005). The resultant expression plasmid p35S::SePSY1-mYFP driven under 35S promoter was transferred into Agrobacterium Khan et al (2009).…”