Histopathology of infection and colonization of Quercus ilex fine roots by Phytophthora cinnamomi

Abstract

Quercus ilex is one of the European forest species most susceptible to root rot caused by the oomycete Phytophthora cinnamomi. This disease contributes to holm oak decline, a particularly serious problem in the 'dehesas' ecosystem of the southwestern Iberian Peninsula. This work describes the host-pathogen interaction of Q. ilex and P. cinnamomi, using new infection indices at the tissue level. Fine roots of 6-month-old saplings inoculated with P. cinnamomi were examined by light microscopy and a random pool of images was analysed in order to calculate different indices based on the measured area of pathogen structures. In the early stages of invasion, P. cinnamomi colonizes the apoplast and penetrates cortical cells with somatic structures. On reaching the parenchymatous tissues of the central cylinder, the pathogen develops different reproductive and survival structures inside the cells and then expands through the vascular system of the root. Some host responses were identified, such as cell wall thickening, accumulation of phenolic compounds in the middle lamella of sclerenchyma tissues, and mucilage secretion blocking vascular cells. New insights into the behaviour of P. cinnamomi inside fine roots are described. Host responses fail due to rapid expansion of the pathogen and a change in its behaviour from biotrophic to necrotrophic.

Histology of Quercus ilex roots during infection by Phytophthora cinnamomi

“…9 inoculation method interaction reported by Haque and Diez (2012). Using the dip method with a suspension of P. cinnamomi chlamydospores, at 3 dpi all tissues of secondary Q. ilex roots were colonized, but first aerial symptoms consisted of leaf discolouration by 14 dpi (Ruiz Gómez et al 2015). Root dip into a zoospore suspension mimics the process that occurs in nature, probably better than the mycelium-root contact method.…”

“…The presence of haustoria, i.e. structures involving feeding relationships between the host and the pathogen (Judelson and Blanco 2005), and the formation of numerous chlamydospores indicate that P. cinnamomi may temporarily behave as a biotrophic pathogen (Crone et al 2013a;Ruiz Gómez et al 2015). It was recently postulated that a necrotrophic mode of P. cinnamomi growth would not provide enough nutrients to produce the large numbers of chlamydospores (Crone et al 2013a).…”

“…Histology of secondary roots of 6-month-old Q. ilex seedlings revealed alterations of the structure of the tissues when trees were inoculated with P. cinnamomi (Ruiz-Gómez et al 2012. Changes in the host included cell wall thickening, an increase in the number and size of intercellular spaces in the central cylinder, accumulation of phenolic compounds in the middle lamella and of pectic substances which sealed pits of the xylem vessels, and the formation of lignitubers (Ruiz Gómez et al 2015). Lignitubers have been recently described as structures in response to P. cinnamomi infection able to isolate cells from penetrating hyphae, even though these encasements alone do not prevent colonization of the host by the pathogen (Crone et al 2013a;Jung et al 2013).…”

“…Lignitubers have been recently described as structures in response to P. cinnamomi infection able to isolate cells from penetrating hyphae, even though these encasements alone do not prevent colonization of the host by the pathogen (Crone et al 2013a;Jung et al 2013). Structures of the pathogen included chlamydospores forming inside the cortex cells, and stromata within the vascular cylinder (Ruiz Gómez et al 2015). Stromata are hyphae which aggregate randomly inside the host (Willetts 1997) and are thought to be involved in the long-term survival of P. cinnamomi in natural environments (Crone et al 2013a, b;Jung et al 2013).…”

Induction of defence responses by cinnamomins against Phytophthora cinnamomi in Quercus suber and Quercus ilex subs. rotundifolia

“…Previous cytohistological observations have shown that P. cinnamomi colonizes Q. suber and Q. ilex penetrating to the phloem and xylem vessels and leading to occlusion, at least in 2-to 6-month-old plants (Pires et al 2008;Horta et al 2010;Medeira et al 2012a;Ruiz-Gómez et al 2014). In addition, recent cytological and physiological studies showed that cryptogein (elicitin secreted by Phytophthora cryptogea) and capsicein (secreted by Phytophthora capsici) induced a resistance response on cork oak against infection by P. cinnamomi (Medeira et al 2012a) and that α-CIN has the same effect in Castanea sativa (Medeira et al 2012b).…”