The Ectomycorrhizal FungusLaccaria bicolorStimulates Lateral Root Formation in Poplar and Arabidopsis through Auxin Transport and Signaling

Abstract

The early phase of the interaction between tree roots and ectomycorrhizal fungi, prior to symbiosis establishment, is accompanied by a stimulation of lateral root (LR) development. We aimed to identify gene networks that regulate LR development during the early signal exchanges between poplar (Populus tremula 3 Populus alba) and the ectomycorrhizal fungus Laccaria bicolor with a focus on auxin transport and signaling pathways. Our data demonstrated that increased LR development in poplar and Arabidopsis (Arabidopsis thaliana) interacting with L. bicolor is not dependent on the ability of the plant to form ectomycorrhizae. LR stimulation paralleled an increase in auxin accumulation at root apices. Blocking plant polar auxin transport with 1-naphthylphthalamic acid inhibited LR development and auxin accumulation. An oligoarray-based transcript profile of poplar roots exposed to molecules released by L. bicolor revealed the differential expression of 2,945 genes, including several components of polar auxin transport (PtaPIN and PtaAUX genes), auxin conjugation (PtaGH3 genes), and auxin signaling (PtaIAA genes). Transcripts of PtaPIN9, the homolog of Arabidopsis AtPIN2, and several PtaIAAs accumulated specifically during the early interaction phase. Expression of these rapidly induced genes was repressed by 1-naphthylphthalamic acid. Accordingly, LR stimulation upon contact with L. bicolor in Arabidopsis transgenic plants defective in homologs of these genes was decreased or absent. Furthermore, in Arabidopsis pin2, the root apical auxin increase during contact with the fungus was modified. We propose a model in which fungus-induced auxin accumulation at the root apex stimulates LR formation through a mechanism involving PtaPIN9-dependent auxin redistribution together with PtaIAA-based auxin signaling.Most temperate forest trees develop a mutualistic root symbiosis with ectomycorrhizal soil fungi. During the establishment of ectomycorrhiza (ECM), fungal hyphae invade the root from root cap cells in and upwards to the epidermis (Horan et al., 1988). After attachment to epidermal cells, hyphae multiply to form a series of layers that differentiate to establish a mantle structure around the root (Horan et al., 1988). An internal network of hyphae between the epidermis and root cortex cells forms the Hartig net (Blasius et al., 1986), while extraradical hyphae prospect throughout the surrounding soil and gather nutrients. Morphological observations of forming ECMs have shown that in the vicinity of the fungus the root architecture of the host plant is profoundly modified. Interaction with hyphae stimulates lateral root (LR) formation, dichotomy of the root apical meristem in conifer species, and cytodifferentiation of root cells (radial elongation and root hair decay; Horan et al., 1988;Dexheimer and Pargney, 1991;. Even though several studies have focused on LR stimulation during ECM formation, it still remains unclear what the molecular mechanisms are that modify root development during contact with the fungus.In the ...

Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes

“…Pathogens, such as P. syringae and H. arabidopsidis, attempt to manipulate the plant response by producing effectors that target different components of the JA (i.e., JAZ proteins) and ET signaling pathways (i.e., ERF proteins) in such a fashion that colonization is favored (10,11,23,24). Like pathogenic bacteria, mutualistic fungi affect plant hormone signaling cascades to achieve colonization (31)(32)(33)(34)(35), although the knowledge of the mechanistic reasoning behind most of these differences is in its infancy. We demonstrate here that MiSSP7, an effector protein produced by 0013s07840 0092s00200 0001s31570 0013s04880 0001s36520 0001s21010 0015s15750 0015s15730 0003s21660 0017s01230 0019s14550 0001s01010 0001s22610 0010s25380 0001s23460 0014s12130 0002s20290 0002s17750 0014s12100 0001s23440 0015s13190 (29), in roots treated with 10 −8 M MeJA (white bars), in two independent transgenic lines expressing MiSSP7 (gray and black bars) and in roots colonized by L. bicolor (stippled bars).…”

“…DivIVa and BiFC interaction tests were used to verify each interaction found in the YTH as per previous reports (28,36). An in vitro assay was used to determine the effects of different chemicals on the ability of L. bicolor S238N to colonize poplar roots after 2 wk of contact between the two organisms as per Felten et al (33). To test if transgenically altering the transcription of PtJAZ6 could complement the loss of MiSSP7 in L. bicolor Δmissp7 RNAi mutants during mycorrhization, we used Agrobacterium rhizogenes strain 15834 to generate stably transformed roots of P. tremula × Populus alba 717-1B4 using a technique similar to that described in Chabaud et al (37).…”

The Role of the Mycorrhizal Symbiosis in Nutrient Uptake of Plants and the Regulatory Mechanisms Underlying These Transport Processes

“…The effect of ECM fungi on lateral root formation is independent from the plant´s ability to form ECM associations. The ECM fungus Laccaria bicolor can induce lateral root formation also in Arabidopsis thaliana, a non-mycorrhizal plant, and the effect is correlated to an accumulation of auxin in the root apices [33]. The auxin accumulation in the root tips and/or other fungal signals could stimulate basipetal auxin transport and lateral root primordia formation by an induction of plant genes involved in auxin transport and signaling.…”

The AINTEGUMENTA LIKE1 Homeotic Transcription Factor PtAIL1 Controls the Formation of Adventitious Root Primordia in Poplar

“…During rooting and growth, cuttings were subirrigated using a hydroponic culture system that has been described previously (Merret et al, 2010). In vitro rooting experiments were performed with the wild type and transgenic lines of Populus tremula 3 Populus alba Institut National de la Recherche Agronomique 717-1B4 and of P. tremula 3 Populus tremuloides Umeä Plant Science Center clone T89 as described previously (Felten et al, 2009;Karlberg et al, 2011). The number of roots per rooted cutting or micropropagated plantlet was estimated throughout the rooting period.…”