Two defined alleles of the LRR receptor kinase GmNARK in supernodulating soybean govern differing autoregulation of mycorrhization

Abstract

Plants regulate the extent of nodulation and root colonization by arbuscular mycorrhizal fungi (AMF), a phenomenon named autoregulation of symbiosis. We tested AMF colonization in split roots of various soybean genotypes [Glycine max (L.) Merr. cv. Bragg, Enrei, Harosoy and Williams], where precolonization of one side of the split‐root system by the AMF Glomus mosseae resulted in reduced mycorrhization of the other. AMF precolonization failed to control secondary mycorrhization in the supernodulating Bragg nonsense mutant nts1007 (Q106*), indicating that the GmNARK gene (predicted to encode a leucine‐rich repeats (LRR) receptor kinase related to CLAVATA1 in Arabidopsis) is involved in autoregulation of the AMF symbiosis. Here, we tested whether the allelic En6500 nonsense supernodulating mutant (GmNARK K606*, derived from cv. Enrei) and supernodulating mutants of cv. Williams (Nod1‐3 and Nod2‐4) with yet‐undefined genetic lesions exhibit a similar symbiotic phenotype in mycorrhizal split‐root systems. Surprisingly, these supernodulating mutants retained their ability to autoregulate AMF. To examine possible differences between two allelic mutants, we determined levels of IAA, abscisic acid, coumestrol, daidzein and genistein in mycorrhizal and uninoculated control roots. Compared with wild‐type plants, both mutants showed reduced IAA accumulation in mycorrhizal roots. Roots of cv. Enrei and En6500 exhibited high levels of isoflavonoids not seen in Bragg or nts1007. Taken together, these findings showed that supernodulation mutants, despite a common nodulation phenotype, differ in their ability to autoregulate AMF root colonization. This suggests either that the GmNARK gene product of some mutants is still partially functional (Q106* vs. K606*) or that varietal differences reflected in altered physiological responses suppress the loss of function.

Community shifts of soybean stem-associated bacteria responding to different nodulation phenotypes and N levels

“…During their evolution, legumes developed nodulation and mycorrhization systems to attain mutual symbiosis with rhizobia and mycorrhizae (Harrison, 2005;Stacey et al, 2006). Although plants are known to control the degrees of nodulation and mycorrhization of roots by rhizobia and mycorrhizae, respectively, through autoregulation systems (Carroll et al, 1985;Meixner et al, 2007), the effects of the autoregulation systems on the other plant-associated microorganisms in the phytosphere remain unclear (Parniske, 2000). Recent studies have shown that the wild-type and symbiosisdefective mutants of legumes such as Medicago truncatula and Glycine max have different microbial community structures, and certain microbes associate preferentially with nodulated or mycorrhizal root systems (Offre et al, 2007;Ikeda et al, 2008a).…”

Nodulation-Dependent Communities of Culturable Bacterial Endophytes from Stems of Field-Grown Soybeans

“…It is well known that the signals involved in both nodulation and mycorrhization overlap in a common signaling pathway, leading to successful symbioses (31,32). Leguminous plants are also known to regulate the degree of nodulation and mycorrhization of roots by rhizobia and mycorrhizae, respectively (3,28). This autoregulatory mechanism occurs through long-distance signaling between the shoot and root (30).…”

Microbial Community Analysis of Field-Grown Soybeans with Different Nodulation Phenotypes

“…AB213415 is a root-associated fungal sequence isolated from the rhizosphere of chrysanthemum. Uncultured basidiomycetes TP1 and TPC2 (accession numbers AY382817 and AY382818) were reported to be orchid mycorrhizae by McCormick et al (16 Fig. 3, the sequences of clones F1 and F4 are more closely related to known species of Auricularia and Exidia/Exidiopsis.…”

“…Plants deficient in autoregulation of nodulation develop hypernodulated roots. In the case of soybean [Glycine max (L.) Merril], hypernodulated mutants differ in their ability to autoregulate root colonization by arbuscular mycorrhizal fungi (16). However, the degree to which plants use similar or identical systems, such as a common signaling pathway and autoregulation, for interactions with other microorganisms remains unclear (23).…”

“…Plants are also known to control the degrees of nodulation and mycorrhization of roots by rhizobia and mycorrhizae, respectively (4,16). This autoregulatory mechanism occurs through long-distance signaling between the shoot and the root (20).…”