Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 67 (15), 4559-70

Redirection of Auxin Flow in Arabidopsis Thaliana Roots After Infection by Root-Knot Nematodes

Affiliations

Redirection of Auxin Flow in Arabidopsis Thaliana Roots After Infection by Root-Knot Nematodes

Tina Kyndt et al. J Exp Bot.

Abstract

Plant-parasitic root-knot nematodes induce the formation of giant cells within the plant root, and it has been recognized that auxin accumulates in these feeding sites. Here, we studied the role of the auxin transport system governed by AUX1/LAX3 influx proteins and different PIN efflux proteins during feeding site development in Arabidopsis thaliana roots. Data generated via promoter-reporter line and protein localization analyses evoke a model in which auxin is being imported at the basipetal side of the feeding site by the concerted action of the influx proteins AUX1 and LAX3, and the efflux protein PIN3. Mutants in auxin influx proteins AUX1 and LAX3 bear significantly fewer and smaller galls, revealing that auxin import into the feeding sites is needed for their development and expansion. The feeding site development in auxin export (PIN) mutants was only slightly hampered. Expression of some PINs appears to be suppressed in galls, probably to prevent auxin drainage. Nevertheless, a functional PIN4 gene seems to be a prerequisite for proper nematode development and gall expansion, most likely by removing excessive auxin to stabilize the hormone level in the feeding site. Our data also indicate a role of local auxin peaks in nematode attraction towards the root.

Keywords: AUX1; Arabidopsis; LAX3; PIN; auxin; galls; root-knot nematode..

Figures

Fig. 1.
Fig. 1.
Promoter activity of Arabidopsis auxin transporter genes in uninfected roots (UR) and in young M. incognita-induced galls at 3 DAI. (A, B) AUX1pro:GUS UR and 3 DAI, (C, D) LAX3pro:GUS UR and 3 DAI, (E, F) PIN1pro:GUS UR and 3 DAI, (G, H) PIN2pro:GUS UR and 3 DAI, (I, J) PIN3pro:GUS UR and 3 DAI, (K, L) PIN4pro:GUS UR and 3 DAI, (M, N) PIN7pro:GUS UR and 3 DAI. Arrows point to the basipetal part of the gall where AUX1, LAX3, and PIN3 expression is activated. G, gall; n, nematode. Bars = 100 µm.
Fig. 2.
Fig. 2.
Promoter activity of Arabidopsis auxin transporter genes in uninfected roots (UR) and in M. incognita-induced galls at 3–14 DAI. (A) AUX1pro:GUS in UR and (B, C) galls at 3 and 7 DAI, (D) LAX3pro:GUS in UR and (E, F) galls at 3 and 7 DAI, (G, I) PIN1pro:GUS in galls at 3, 7, and 14 DAI, (J, K) PIN2pro:GUS at 7 and 14 DAI, (L, M) PIN3pro:GUS at 7 and 14 DAI, (N, O) PIN4pro:GUS at 7 and 14 DAI, (P, Q) PIN7 pro:GUS at 7 and 14 DAI. Arrows point to the basipetal part of the gall where LAX3 and PIN3 expression is activated. GUS staining is visualized in red. C, cortex; Ep, epidermis; n, nematode; NC, neighbouring cells; RAM, root apical meristem; asterisk, giant cell. Bars = 50 µm.
Fig. 3.
Fig. 3.
PIN1pro:PIN1-GFP, PIN2pro:PIN2-GFP, PIN3pro:PIN3-GFP, PIN4pro:PIN4-GFP, and PIN7pro:PIN7-GFP analysis in uninfected roots and in M. incognita-induced galls at 3, 7, and 10 DAI in Arabidopsis. Arrows point to the accumulation of PIN1-GFP, PIN3-GFP, and PIN7-GFP at the acropetal side of cells. C, cortex; G, gall; n, nematode; NC, neighbouring cells; UR, uninfected root; asterisk, giant cell. Bars = 25 µm.
Fig. 4.
Fig. 4.
Analyses of pin1 Arabidopsis mutant and its corresponding wild type En-2, infected by the RKN M. incognita. (A) Number of J2 per plant, counted at 3 (dark grey) and 7 DAI (light grey). Different letters indicate statistically significant differences based on a Student’s t-test (P < 0.05), using upper case for 3 DAI and lower case for 7 DAI. (B) Number of galls at 35 DAI. Different letters indicate statistically significant differences based on a Student’s t-test (P < 0.05). (C) Developmental stages of the observed nematodes within the galls at 42 DAI, shown as percentages. (D) Classification of gall sizes at 35 DAI, shown as percentages. Extra-large (> 2.5mm), large galls (1.5–2.5mm), medium galls (1–1.5mm), and small galls (<1mm). In A and B, bars represent the average ± standard deviation of at least 10 individual plants. The whole infection experiment was twice independently repeated, giving similar results. In C and D, bars represent the percentage of each developmental stage (of ~400 nematodes per line) or gall size (of ~250 galls per line) counted on all 10 individual plants in one infection experiment.
Fig. 5.
Fig. 5.
Analyses of aux1, lax3, aux1 lax3, pin2, pin3, and pin4 Arabidopsis mutants infected by the RKN M. incognita. (A) Number of J2 per plant, counted at 3 and 7 DAI. Different letters indicate statistically significant differences based on ANOVA and Tukey’s test (P < 0.05), using upper case for 3 DAI and lower case for 7 DAI. (B) Number of galls at 35 DAI. Different letters indicate statistically significant differences (P < 0.05). (C) Developmental stages of the observed nematodes within the galls 42 DAI, shown as percentages. (D) Classification of gall sizes at 35 DAI, shown as percentages. Extra-large (> 2.5mm), large galls (1.5–2.5mm), medium galls (1–1.5mm), and small galls (<1mm). In A and B, bars represent the average ± standard deviation of at least 10 individual plants. The whole infection experiment was twice independently repeated, giving similar results. In C and D, bars represent the percentage of each developmental stage (of ~400 nematodes per line) or gall size (of ~250 galls per line) counted on all 10 individual plants in one infection experiment.
Fig. 6.
Fig. 6.
Model of AUX1/LAX3/PIN-mediated auxin transport during nematode feeding site development, based on the 3 and 7 DAI data provided in this manuscript. The giant cells are shown as yellow circles, and the nematode is the green-brown worm. Grey arrows show the direction of the auxin flow in uninfected Arabidopsis roots, and the auxin import/export proteins that are mainly responsible for this flow (based on Feraru and Friml, 2008). Orange arrows show the redirected auxin flow in nematode feeding sites, based on the data provided in this study. n, nematode; brown stars, nematode-secreted auxin. This figure is available in colour at JXB online.

Similar articles

See all similar articles

Cited by 12 articles

See all "Cited by" articles

References

    1. Abas L, Benjamins R, Malenica N, Paciorek T, Wirniewska J, Moulinier-Anzola JC, Sieberer T, Friml J, Luschnig C. 2006. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nature Cell Biology 8, 249–256. - PubMed
    1. Absmanner B, Stadler R, Hammes UZ. 2013. Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin. Frontiers in Plant Science 4, 241. - PMC - PubMed
    1. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J. 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602. - PubMed
    1. Curtis RHC. 2007. Do phytohormones influence nematode invasion and feeding site establishment? Nematology 9, 155–160.
    1. De Smet I, Lau S, Voss U, et al. 2010. Bimodular auxin response controls organogenesis in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 107, 2705–2710. - PMC - PubMed

Publication types

MeSH terms

Feedback