New symptoms identified in phytoplasma-infected plants reveal extra stages of pathogen-induced meristem fate-derailment

Authors: Wei, Wei; Davis, Robert; Bauchan, Gary; Zhao, Yan

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/14/2019
Publication Date: 5/23/2019
Citation: Wei, W., Davis, R.E., Bauchan, G.R., Zhao, Y. 2019. New symptoms identified in phytoplasma-infected plants reveal extra stages of pathogen-induced meristem fate-derailment. Molecular Plant-Microbe Interactions. https://doi.org/10.1094/MPMI-01-19-0035-R.
DOI: https://doi.org/10.1094/MPMI-01-19-0035-R

Interpretive Summary: Over the life cycle of a flowering plant, stem cells in shoot tips (shoot apical meristems) undergo a graduated, multi-stage transition from vegetative to reproductive destiny. In a previous study, we found that such natural transition can be disrupted by phytoplasma, a tiny bacterium that parasitizes nutrient-conducting vessels of host plants. We showed that phytoplasma-induced abnormal morphogenesis of flowers reflects stage-specific derailment of shoot apical meristems from their genetically preprogrammed reproductive destiny. Our current study unveiled new phytoplasmal disease symptoms that developed over the course of flower formation, fruit setting, and seed germination, pointing to derailment of the meristem fate at additional stages previously unknown. Our findings lead us hypothesize that multiple phytoplasmal virulence factors are present and that each act at a specific stage in the meristem transition. The study provides a framework for identifying such developmental stage-specific virulence factors. The information is important to scientists who are studying plant growth and development, pathogen-host interactions, and molecular basis of diseases. This article will also be of interest to biotechnologists and agricultural economists who are concerned with phytoplasmal disease symptom management.

Technical Abstract: In flowering plants, the transition of a shoot apical meristem from vegetative to reproductive destiny is a graduated, multi-stage process that involves sequential conversion of the vegetative meristem (VM) to an inflorescence meristem (IF), initiation of floral meristems (FMs), emergence of flower organ primordia, and formation of four whorls of floral organs. As critical as it is for survival of the species, this orderly process can be derailed by phytoplasma, a mycoplasma-like microbe that parasitizes phloem cells of diverse flowering plants. In a previous study, we showed that phytoplasma-induced abnormal morphogenesis of flowers reflects stage-specific derailment of shoot apical meristems from their genetically preprogrammed reproductive destiny. Our current study of phytoplasmal infection in an early flowering tomato genotype made it possible to unveil new symptoms of abnormal morphogenesis (parthenocarpy and floral duplication), pointing to derailment of flower development/meristem transition at additional stages not identified previously. We also found that the fate of developing meristems may be derailed even after normal termination of floral meristem and onset of seed production, causing vivipary. While previous reports by others have indicated that different symptoms may be induced by different phytoplasmal pathogenicity factors (effectors), our findings lead us hypothesize (i) that effectors act at specific stages of meristem development/transition, and (ii) that specific floral abnormalities may be attributable to meristem fate-derailment by different effectors that each act at a specific stage in meristem transition. These hypotheses predict that an array of yet-undiscovered effectors will be found; this study provides a framework for identifying such developmental stage-specific phytoplasmal effectors.