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Title: Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture

Author
item Wei, Wei
item Davis, Robert
item NUSS, DONALD - University Of Maryland
item Zhao, Yan

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/17/2013
Publication Date: 11/4/2013
Citation: Wei, W., Davis, R.E., Nuss, D.F., Zhao, Y. 2013. Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture. Proceedings of the National Academy of Sciences. 110:19149-19154.

Interpretive Summary: In higher plants, it is the fate of stem cells (termed meristems) that determines the pattern of plant growth, and therefore plant shape and fruitfulness. The conversion of the meristems from vegetative state to floral initial is a critical event that decides whether a flowering plant will produce the next generation of seeds. In nature, as well as in agriculture, this event assumes greater importance for survival of a plant species through a non-growing season as well as for survival of other members of a biosphere. We discovered that a bacterial infection can derail such an important process by diverting the meristems from their normal destiny. We identified four symptoms in tomato plants infected with a phytoplasma (a cell wall-less bacterium), and found that each symptom corresponds to a distinct phase in the derailment of meristem fate. We unveiled major molecular events beneath the pathogen-induced meristem fate derailment and proposed a model to explain such a striking phenomenon. Our findings open a new avenue toward understanding pathological alterations in patterns of plant growth and development thus aiding in identification of molecular targets for disease control and symptom management. The findings also raise a possibility for using phytoplasma as a tool to study the course of normal plant development and to modify plant growth by manipulating meristem fate. The information is important to research scientists, students, and university professors 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 disease symptom management and food security.

Technical Abstract: In the life cycle of higher plants, it is the fate of meristem cells that determines the pattern of growth and development, and therefore plant morphotype and fertility. Floral transition, the turning point from vegetative growth to reproductive development, is achieved via genetically-programmed sequential changes in meristem fate from vegetative to inflorescence, and to floral, leading to flower formation and eventual seed production. The transition is rarely reversible once initiated. In this communication, we report that a bacterial infection can derail the genetically programmed fate of meristem cells, thereby drastically altering the growth pattern of the host plant. We identified four characteristic symptoms in tomato plants infected with a cell wall-less bacterium, phytoplasma. The symptoms are a manifestation of the pathogen-induced floral reversion and vegetative proliferation (here termed PIFR-VP) whereas each symptom corresponds to a distinct phase in the derailment of shoot apical meristem fate. The phases include premature floral meristem termination, suppressed floral meristem initiation, delayed vegetative to inflorescence meristem conversion, and repetitive initiation of lateral vegetative meristems. We further found that the PIFR-VP was correlated with transcriptional reprogramming of key meristem switching genes. Our findings open an avenue toward understanding pathological alterations in patterns of plant growth and development thus aiding in identification of molecular targets for disease control and symptom alleviation. The findings also raise a tantalizing possibility for using phytoplasma as a tool to dissect the course of normal plant development and to modify plant morphogenesis by manipulating meristem fate.