Auxin transport inhibitors act through ethylene to regulate dichotomous branching of lateral root meristems in pine

Abstract

Many soil fungi colonize the roots of pines to form symbiotic organs known as ectomycorrhizas. Dichotomous branching of short lateral roots and the formation of coralloid organs are diagnostic of ectomycorrhizas in many pine species, although the regulation of these changes in root morphology is not well understood. We used axenic root cultures of six pine species to examine the role of auxin, cytokinin, ethylene and nutrients in the regulation of root architecture. Surprisingly, extensive dichotomous and coralloid branching of lateral roots occurred spontaneously in Pinus taeda, P. halepensis and P. muricata. In P. sylvestris, P. ponderosa and P. nigra, treatment with auxin transport inhibitors (ATIs), the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) or the ethylene-releasing compound 2-chloroethylphosphonic acid (CEPA or ethephon) induced extensive dichotomous branching and coralloid organ formation. Formation of both spontaneous and ATI-induced coralloid structures was blocked by treatment with an ethylene synthesis inhibitor L-α-(2-aminoethoxyvinyl)glycine ; this inhibition was reversed by either ACC or CEPA. In addition, the induction of this unique morphogenetic pattern in pine root cultures was regulated by nutrient levels. The morphology and anatomical organization of the chemically induced dichotomous and coralloid structures, as well as the regulation of their formation by nutrient levels, show a striking similarity to those of ectomycorrhizas.

The Ethylene-InsensitivesickleMutant ofMedicago truncatulaShows Altered Auxin Transport Regulation during Nodulation

“…As another example, ethylene-insensitive root 1 (allelic to pin2) shows a defect in gravitropic response and a reduced sensitivity to ethylene (Roman et al, 1995) and the auxin transport inhibitor NPA (Luschnig et al, 1998). These studies in Arabidopsis and studies in pine (Kaska et al, 1999) suggest that some of the effects of ethylene are via regulation of polar auxin transport and in turn, auxin transport regulation often requires ethylene signaling.…”

Communication and Signaling in the Plant–Fungus Symbiosis: The Mycorrhiza

“…The production of hormones, including auxins, cytokinins, abscisic acid and ethylene, by ectomycorrhizal fungi was first reported in the early 1990s (Gogala 1991) . Many studies indicate that changes in auxin balance are a prerequisite for mycorrhiza organogenesis (Rupp et al 1989 ;Gay et al 1994 ;Karabaghli-Degron et al 1998 ;Kaska et al 1999) (e.g., short root development). The presence of plantderived molecules in the rhizosphere could be sufficient to enhance the biosynthesis of hormones by ectomycorrhizal fungi (Rupp et al 1989) , which induce morphological changes leading to symbiosis development.…”

Dichotomization of mycorrhizal and NPA-treated short roots inPinus sylvestris

“…1A and B). In addition to NPA, precursors of ethylene synthesis 13 and ethylene itself 17 have been shown to induce dichotomization of short roots comparable to those in mycorrhiza. A similar phenotype is suggested to result from the activation of ethylene biosynthesis by the increased auxin concentration, 13 caused by NPA-treatment at the root tip.…”

“…In addition to NPA, precursors of ethylene synthesis 13 and ethylene itself 17 have been shown to induce dichotomization of short roots comparable to those in mycorrhiza. A similar phenotype is suggested to result from the activation of ethylene biosynthesis by the increased auxin concentration, 13 caused by NPA-treatment at the root tip. 19,20 The new reports dealing with the hormonal regulation of root growth in Arabidopsis draw attention to the complicated relationship prevailing between ethylene and auxin signaling, 4-7 which could also be the acting factor behind the P. sylvestris short root morphogenesis.…”

“…9 The factors regulating the limited growth of the short roots, their ability to host fungal mycelium and the morphological changes at ectomycorrhizal symbiosis have interested the researchers for years. 8,[10][11][12][13][14][15] The formation of dichotomous roots has been suggested to result from changes in either auxin or ethylene concentrations due to the fungal growth in the root. [15][16][17][18] …”