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, 5 (1), e1000266

Parasitic Nematodes Modulate PIN-mediated Auxin Transport to Facilitate Infection

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Parasitic Nematodes Modulate PIN-mediated Auxin Transport to Facilitate Infection

Wim Grunewald et al. PLoS Pathog.

Abstract

Plant-parasitic nematodes are destructive plant pathogens that cause significant yield losses. They induce highly specialized feeding sites (NFS) in infected plant roots from which they withdraw nutrients. In order to establish these NFS, it is thought that the nematodes manipulate the molecular and physiological pathways of their hosts. Evidence is accumulating that the plant signalling molecule auxin is involved in the initiation and development of the feeding sites of sedentary plant-parasitic nematodes. Intercellular transport of auxin is essential for various aspects of plant growth and development. Here, we analysed the spatial and temporal expression of PIN auxin transporters during the early events of NFS establishment using promoter-GUS/GFP fusion lines. Additionally, single and double pin mutants were used in infection studies to analyse the role of the different PIN proteins during cyst nematode infection. Based on our results, we postulate a model in which PIN1-mediated auxin transport is needed to deliver auxin to the initial syncytial cell, whereas PIN3 and PIN4 distribute the accumulated auxin laterally and are involved in the radial expansion of the NFS. Our data demonstrate that cyst nematodes are able to hijack the auxin distribution network in order to facilitate the infection process.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Expression of PIN genes upon infection with H. schachtii.
(A–C) DR5 activity in NFS at 24 hpi (A), 2 dpi (B) and 5 dpi (C). NFS is outlined in (C). (D,E) PIN1::GUS expression is absent in NFS at 2 dpi (D) and 5 dpi (E). (G,H) PIN2 is not expressed at 2 dpi (G) nor at 5 dpi (H). Inset is close-up of nematode head and feeding site. (F,I) PIN3 is highly expressed at 2 dpi (F) and 5 dpi (I). (J,K) PIN4::GUS expression at 2 dpi (J) and 5 dpi (K). (L,M) PIN7 is not expressed in NFS at 2 dpi (L) nor at 5 dpi (M). Single arrowheads point to nematode heads; double headed arrows indicate NFS when not GUS-stained.
Figure 2
Figure 2. PIN3-GFP localisation upon infection with H. schachtii.
(A) Merged GFP and transmission confocal image of a syncytium at 4 dpi. (B) Detail of (A) showing basal localisation in vascular tissue and lateral localisation in the syncytium. (C) Uninfected PIN3::PIN3-GFP control root showing basal PIN3-GFP localisation of pericycle cells. N, nematode; s, syncytium; arrows show asymmetric PIN localisation.
Figure 3
Figure 3. Infection studies of pin mutants using the cyst nematode H. schachtii.
(A) Number of cysts in percentage obtained from several pin mutants six weeks after inoculation. Asterisks point to significant values (p<0.05). (B) Number of cysts in percentage obtained from several pin mutants six weeks after inoculation and divided in different categories. For the “very small cysts” category, the mutants were statiscally grouped in several classes (a–d; p<0.05). (C) Different categories of cysts obtained from infection experiments on pin mutants. Both length and width of the cysts were measured. n = number of cysts measured.
Figure 4
Figure 4. Model of PIN-mediated auxin transport during NFS establishment.
(A) Uninfected root cells. (B) In response to nematode infection PIN1 expression is downregulated in the initial feeding cell, thus hampering PIN1-mediated basipetal auxin transport, and as a result auxin accumulates in this cell. (C) In order to expand their feeding site radially, nematodes direct PIN3 to the lateral cell membranes and consequently auxin is transported laterally towards the surrounding cells. Red lines represent PIN1; green lines represent PIN3; arrows indicate auxin flow; blue colouring illustrates DR5-visualized auxin response.

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