Phloem-and xylem-restricted plant pathogenic bacteria

This review concerns plant pathogenic bacteria, which are strictly restricted either to the sieve tubes in the phloem or to the vessels in the xylem. These bacteria are endogenous as opposed to exogenous bacteria such as species of Erwinia , Pseudomonas , Ralstonia or Xanthomonas , which colonize the apoplast (intercellular spaces) of plant tissues, even though some of the exogenous bacteria, such as Xylophilus ampelina , can also induce vascular infections. Due to their vascular habitat, the endogenous bacteria have a systemic distribution throughout the plant, they are transmitted from plant to plant by graft inoculation, and most of them are vectored by insects which feed in the phloem (leafhoppers, psyllids), or the xylem (sharpshooters). Because of these virus-like properties, the diseases caused by endogenous bacteria have long been taken for virus diseases. The principal conducting cells of the phloem are the sieve tube elements [37]. These elements are joined end to end into sieve tubes, and are associated with parenchymatic, nucleated cells, the companion cells, an important role of which is to load sucrose into the sieve tubes. The sieve tube elements are living cells, which become enucleated at maturity. The sieve plates are lateral wall areas between two adjacent sieve elements. The sieve plates are clustered with pores, resembling giant plasmodesmata and interconnecting two adjacent sieve elements through their cytoplasms. The diameter of a pore ranges from a fraction of a micron (m) to 15 m and more, and is large enough to allow passage of sieve tube-restricted bacteria. The principal conducting elements of the xylem are tracheids and vessel members [37]. Both are dead cells, contain no cytoplasm, and have lignified secondary walls. The vessel elements are joined end to end into vessels, and the adjoining ends have open perforation plates. These openings allow relatively unimpeded longitudinal spread of the xylem-restricted bacteria within the vessels. On the lateral walls, both tracheids and vessel members have apertures, called pits, which have membranes separating adjoining elements. Lateral movement of xylem-restricted bacteria through pits implies breaching pit membranes. Most phloem-restricted bacteria have resisted in vitro cultivation, even though they multiply actively in phloem sap within the sieve tubes. This suggests that the rich phloem sap, in contrast to culture media, contains nutrients still to be identified and indispensable for the growth of phloem-restricted bacteria. The xylem sap is not as rich as phloem sap, and most xylemrestricted bacteria can be cultured in vitro. The discovery of endogenous bacteria began with sieve tube-restricted organisms. The first were seen in Japan in 1967 [35], and were particular in that they lacked a cell wall. They resembled a group of wall-less bacteria, the mycoplasmas or mollicutes, known as human and animal pathogens, and first cultured as early as 1898 [87]. Therefore, the newly discovered sieve tube-restricted organisms became known as mycoplasma-like organisms or MLOs, now called ‘phytoplasmas’. The spiroplasmas were discovered in 1970. While the phytoplasmas have no defined morphology, the spiroplasmas are helical organisms, and this welldefined morphology, for organisms lacking a cell wall, came as a surprise. In addition to wall-less bacteria (phytoplasmas and spiroplasmas), sieve tubes may also contain walled bacteria of the Gram-negative type (proteobacteria). The best-studied ones are the liberibacters and the phlomobacters. The liberibacters were discovered in 1970 [75] through the study of citrus greening disease, now renamed ‘huanglongbing’. Marginal chlorosis of strawberries led to the discovery of phlomobacters in 1993 [88,127]. * Corresponding author. Tel.: /33-5-57-12-23-55; fax: /33-5-5684-31-59 E-mail address: [email protected] (J.M. Bové). Plant Science 163 (2002) 1083 /1098