Abstract

Background‘Candidatus Phytoplasma solani’ is endemic in Europe and infects a wide range of weeds and cultivated plants. Phytoplasmas are prokaryotic plant pathogens that colonize the sieve elements of their host plant, causing severe alterations in phloem function and impairment of assimilate translocation. Typical symptoms of infected plants include yellowing of leaves or shoots, leaf curling, and general stunting, but the molecular mechanisms underlying most of the reported changes remain largely enigmatic. To infer a possible involvement of Fe in the host-phytoplasma interaction, we investigated the effects of ‘Candidatus Phytoplasma solani’ infection on tomato plants (Solanum lycopersicum cv. Micro-Tom) grown under different Fe regimes.ResultsBoth phytoplasma infection and Fe starvation led to the development of chlorotic leaves and altered thylakoid organization. In infected plants, Fe accumulated in phloem tissue, altering the local distribution of Fe. In infected plants, Fe starvation had additive effects on chlorophyll content and leaf chlorosis, suggesting that the two conditions affected the phenotypic readout via separate routes. To gain insights into the transcriptional response to phytoplasma infection, or Fe deficiency, transcriptome profiling was performed on midrib-enriched leaves. RNA-seq analysis revealed that both stress conditions altered the expression of a large (> 800) subset of common genes involved in photosynthetic light reactions, porphyrin / chlorophyll metabolism, and in flowering control. In Fe-deficient plants, phytoplasma infection perturbed the Fe deficiency response in roots, possibly by interference with the synthesis or transport of a promotive signal transmitted from the leaves to the roots.Conclusions‘Candidatus Phytoplasma solani’ infection changes the Fe distribution in tomato leaves, affects the photosynthetic machinery and perturbs the orchestration of root-mediated transport processes by compromising shoot-to-root communication.

Highlights

  • Phytoplasmas are plant pathogenic bacteria belonging to the class Mollicutes, a group of wall-less and pleomorphic microorganisms [1], which live a trans-kingdom parasitic life, infecting both plants and phloem-feeding insect hosts [2]

  • Upon Fe-starvation, infected plants (I/−Fe plants) developed symptoms of both stresses, i.e. yellowing and surface reduction of leaves, the typical phytoplasma-induced alterations of shoots and flowers, as well as the root modifications caused by Fe deficiency (Fig. 1d, f, g)

  • Fe starvation and phytoplasma infection induce specific, partially overlapping changes in the transcriptome of tomato leaves To gain insights into the transcriptional response to phytoplasma infection or Fe deficiency, single-end stranded RNA sequencing (RNA-seq) transcriptome profiling was performed on midrib-enriched leaves

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Summary

Introduction

Phytoplasmas are plant pathogenic bacteria belonging to the class Mollicutes, a group of wall-less and pleomorphic microorganisms [1], which live a trans-kingdom parasitic life, infecting both plants and phloem-feeding insect hosts [2]. Buoso et al BMC Genomics (2019) 20:703 strongly reduced metabolic capabilities and must absorb essential compounds from their hosts. This observation is supported by the presence of multiple copies of transportrelated genes such as malate, metal-ion, and amino acid transporters in the phytoplasma genome [14]. Phytoplasma-infected plants often exhibit a variety of symptoms, including virescence, phyllody, witches’-broom growth (proliferation of auxiliary or axillary shoots), abnormal elongation of internodes, flower malformation, and sterility. Yellowing of leaves or shoots, leaf curling, and general stunting are typical symptoms of infected plants, often associated with reduced content of chlorophyll, carotenoids, and proteins of light-harvesting complexes (LHC) [32, 33]. Some symptoms represent a derailment of programmed meristem fate and a modified pattern of growth due to pathogen-affected key meristem switching genes [34, 35]; the molecular mechanisms underlying most of the reported changes remain, largely enigmatic

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