Acropetal Auxin Transport Inhibition Is Involved in Indeterminate But Not Determinate Nodule Formation

Abstract

Legumes enter into a symbiotic relationship with nitrogen-fixing rhizobia, leading to nodule development. Two main types of nodules have been widely studied, indeterminate and determinate, which differ in the location of the first cell division in the root cortex, and persistency of the nodule meristem. Here, we compared the control of auxin transport, content, and response during the early stages of indeterminate and determinate nodule development in the model legumes Medicago truncatula and Lotus japonicus, respectively, to investigate whether differences in auxin transport control could explain the differences in the location of cortical cell divisions. While auxin responses were activated in dividing cortical cells during nodulation of both nodule types, auxin (indole-3-acetic acid) content at the nodule initiation site was transiently increased in M. truncatula, but transiently reduced in L. japonicus. Root acropetal auxin transport was reduced in M. truncatula at the very start of nodule initiation, in contrast to a prolonged increase in acropetal auxin transport in L. japonicus. The auxin transport inhibitors 2,3,5-triiodobenzoic acid and 1-N-naphthylphthalamic acid (NPA) only induced pseudonodules in legume species forming indeterminate nodules, but failed to elicit such structures in a range of species forming determinate nodules. The development of these pseudonodules in M. truncatula exhibited increased auxin responses in a small primordium formed from the pericycle, endodermis, and inner cortex, similar to rhizobia-induced nodule primordia. In contrast, a diffuse cortical auxin response and no associated cortical cell divisions were found in L. japonicus. Collectively, we hypothesize that a step of acropetal auxin transport inhibition is unique to the process of indeterminate nodule development, leading to auxin responses in pericycle, endodermis, and inner cortex cells, while increased auxin responses in outer cortex cells likely require a different mechanism during the formation of determinate nodules.

Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation

“…Although auxin response genes are induced at the site of initiation of both determinate and indeterminate nodules, the inhibition of polar auxin transport is crucial for indeterminate but not determinate nodule development ( Figure 6; Ng and Mathesius, 2018). Medicago PINFORMED (PIN) auxin exporters MtPIN2, MtPIN3, and MtPIN4 and the auxin influx carrier MtLAX2 (LIKE AUXIN2) promote nodule organogenesis (Huo et al, 2006;Roy et al, 2017).…”

Mini-Review: Nod Factor Regulation of Phytohormone Signaling and Homeostasis During Rhizobia-Legume Symbiosis

“…We present data from legumes producing both indeterminate ( Medicago truncatula , pea) and determinate [ Lotus japonicus , Glycine max (soybean)] nodules. These two types of nodule differ in the site of initial cortical divisions, persistency of the nodule meristem and auxin sensitivity ( Bensmihen, 2015 ; Ng and Mathesius, 2018 ). Effects of NF signaling on both hormone homeostasis and hormone signaling will be discussed.…”

Biological activity of Nod factors

“…In the case of M. truncatula plants, Nod factor application or infection by S. meliloti cells inhibited auxin transport from root to shoot in the first 24 h and this observation coincided with the very earliest cortical cell divisions (Ng et al, 2015). It was suggested that the Nod factors caused inhibition of acropetal auxin transport and probably this is unique to the process of indeterminate nodule organogenesis (Ng & Mathesius, 2018).…”