Recognition of floral homeotic MADS domain transcription factors by a phytoplasmal effector, phyllogen, induces phyllody

Abstract

Plant pathogens alter the course of plant developmental processes, resulting in abnormal morphology in infected host plants. Phytoplasmas are unique plant-pathogenic bacteria that transform plant floral organs into leaf-like structures and cause the emergence of secondary flowers. These distinctive symptoms have attracted considerable interest for many years. Here, we revealed the molecular mechanisms of the floral symptoms by focusing on a phytoplasma-secreted protein, PHYL1, which induces morphological changes in flowers that are similar to those seen in phytoplasma-infected plants. PHYL1 is a homolog of the phytoplasmal effector SAP54 that also alters floral development. Using yeast two-hybrid and in planta transient co-expression assays, we found that PHYL1 interacts with and degrades the floral homeotic MADS domain proteins SEPALLATA3 (SEP3), APETALA1 (AP1) and CAULIFLOWER (CAL). This degradation of MADS domain proteins was dependent on the ubiquitin–proteasome pathway. The expression of floral development genes downstream of SEP3 and AP1 was disrupted in 35S::PHYL1 transgenic plants. PHYL1 was genetically and functionally conserved among other phytoplasma strains and species. We designate PHYL1, SAP54 and their homologs as members of the phyllody-inducing gene family of ‘phyllogens’.

Degradation of class E MADS-domain transcription factors in Arabidopsis by a phytoplasmal effector, phyllogen

“…The Agrobacterium strain and plasmids were the same as in the previous study, respectively. 15 The composition of the infiltration buffer is as follows: 10 mM morpholinepropanesulfonic acid (MES, pH 5.6), 10 mM MgCl 2 , and 150 mM acetosyringone. Nuclear localization of the transcription factors used in this study was confirmed by DAPI staining (data not shown).…”

“…This result agrees well with the fact that transgenic Arabidopsis plants expressing phyllogens show floral homeotic phenotypes similar to those of triple or quadruple mutants of sep genes. 1,4,14,15 Moreover, SEP3-and SEP1/2/4-like genes are highly conserved among various angiosperms as genes of the SEP sub-family encoding class E MADS TFs. 17 Therefore, it is likely that phyllogens broadly target class E proteins of angiosperms, including eudicots, monocots, and other taxa, for degradation.…”

“…12,13 Moreover, an inducer of witches' broom, designated TENGU, and a gene family of phyllody-inducing effectors, designated phyllogens, were identified from phytoplasmas. 12,14,15 Phyllogens interact with and degrade some MADS TFs, including SEP3 of Arabidopsis. 15,16 However, it is unknown whether the other 3 class E proteins (SEP1, SEP2, and SEP4) of Arabidopsis are also degraded by phyllogens, though their interactions with a phyllogen were shown in a yeast 2-hybrid assay.…”

“…12,14,15 Phyllogens interact with and degrade some MADS TFs, including SEP3 of Arabidopsis. 15,16 However, it is unknown whether the other 3 class E proteins (SEP1, SEP2, and SEP4) of Arabidopsis are also degraded by phyllogens, though their interactions with a phyllogen were shown in a yeast 2-hybrid assay. 16 It is also interesting from the perspective of the phylogenetic differences between SEP Keywords: Arabidopsis, floral development, MADS transcription factors, phyllody, phyllogen, phytoplasma, SEPALLATA genes: in an evolutionary analysis of SEP gene sub-family, SEP3 and the other 3 SEP genes of Arabidopsis were divided into 2 different clades.…”

Exploring the phytoplasmas, plant pathogenic bacteria

“…As for phyllody symptoms, a previous study has shown the involvement of the floral homeotic MADS-domain transcription factors of the floral ABCE model (floral quartet model) . Recently, PHYL1 and SAP54 were found to be homologous secreted proteins that induce phyllody in floral organs of Arabidopsis thaliana Maejima et al 2014). PHYL1 actually interacts with and degrades these MADS-domain transcription factors .…”