Tomato Flower Abnormalities Induced by Stolbur Phytoplasma Infection Are Associated with Changes of Expression of Floral Development Genes

Abstract

Tomato (Lycopersicon esculentum cv. Micro-Tom) plants infected by the stolbur phytoplasma (isolate PO) display floral abnormalities, including sepal hypertrophy, virescence, phyllody, and aborted reproductive organs, which are reminiscent of those observed in Arabidopsis thaliana mutants affected in flower development genes. Semiquantitative reverse transcription-polymerase chain reaction and in situ RNA hybridization were used to compare expressions of meristem and flower development genes in healthy and stolbur phytoplasma-infected tomatoes. In infected plants, FALSIFLORA (FA), controlling the identity of the inflorescence meristem, was up-regulated, whereas LeWUSCHEL (LeWUS) and LeCLAVATA1 (LeCLV1), regulating the meristem development, and LeDEFICIENS (LeDEF), responsible for the organ (petals and stamens) identity within the flower, were down-regulated regardless of the development stage of the flower bud. In contrast, expression of TAG1, which regulates stamen and carpel identities and negatively controls LeWUS, was up-regulated at the early stages and down-regulated at the late stages. In situ RNA hybridization analyses revealed that TAG1 transcripts were restricted to the same floral meristem territories in healthy and infected tomatoes, indicating that tissue-specific expression of TAG1 was not affected by the stolbur phytoplasma infection. Taken together, these data indicate that flower malformations of stolbur phytoplasma-infected tomatoes are associated with early changes in the expression of key flower development genes. The possible mechanisms by which the multiplication of stolbur phytoplasma in tomato sieve tubes deregulates floral development are discussed.

Phytoplasma Effector SAP54 Induces Indeterminate Leaf-Like Flower Development in Arabidopsis Plants

“…Although we were unable to identify SAP54 homologs in a number of phytoplasmas known to influence flower architecture (e.g. stolbur phytoplasma; Pracros et al, 2006), our efforts were severely constrained by the limited availability of phytoplasma sequence data; thus, it cannot be concluded that these phytoplasmas do not encode a SAP54-like effector. Conversely, it is possible that these phytoplasmas employ different effectors to modulate flower development in their hosts.…”

“…For example, the production of a secondary flower in place of a carpel (loss of fourth whorl determinacy) indicates that phytoplasmas might interfere in some way with the function of the C-class protein AGAMOUS, and there is evidence that the expression of an AGAMOUS ortholog is altered in tomato (Solanum lycopersicum) infected with stolbur phytoplasma (Pracros et al, 2006). We also notice striking similarities between flowers of AY-WB-infected plants and sep1 sep2 sep3/+ sep4 quadruple mutants (Ditta et al, 2004).…”

“…AGAMOUS is a C-class protein that is involved in stamen and carpel development and in the termination of flower development. Various genes involved in floral organ formation are misregulated in phytoplasma-infected plants (Pracros et al, 2006;Cettul and Firrao, 2010;Himeno et al, 2011). We hypothesized that phytoplasmas produce specific effectors that interfere with floral organ formation (Sugio et al, 2011).…”

cDNA-AFLP analysis of gene expression changes in apple trees induced by phytoplasma infection during compatible interaction

“…By the same techinque, Carginale et al (2004) found only four genes that were differentially expressed in Prunus armeniaca infected by phytoplasma. Using semi-quantitative RT-PCR and in situ RNA hybridization, Pracros et al (2006) found some floral development genes to be differentially regulated in a tomato-stolbur phytoplasma interaction.…”

Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture

“…Plants with phytoplasmal diseases often exhibit symptoms of shoot proliferation, witches'-broom (WB) growth, and flower malformation (13). Studies have revealed that, in deformed flowers of phytoplasma-affected plants, expressions of FM and floral organ identity genes become altered (14)(15)(16)(17) (Table 1). Although such findings provided some insights into molecular events involved in homeotic transformations of floral organs, the underlying response mechanisms that led to phytoplasma-induced multiple morphological abnormalities have remained unexplored.…”