Abstract

Most legume plants can form nodules, specialized lateral organs that form on roots, and house nitrogen-fixing bacteria collectively called rhizobia. The uptake of the phytohormone auxin into cells is known to be crucial for development of lateral roots. To test the role of auxin influx in nodulation we used the auxin influx inhibitors 1-naphthoxyacetic acid (1-NOA) and 2-NOA, which we found reduced nodulation of Medicago truncatula. This suggested the possible involvement of the AUX/LAX family of auxin influx transporters in nodulation. Gene expression studies identified MtLAX2, a paralogue of Arabidopsis (Arabidopsis thaliana) AUX1, as being induced at early stages of nodule development. MtLAX2 is expressed in nodule primordia, the vasculature of developing nodules, and at the apex of mature nodules. The MtLAX2 promoter contains several auxin response elements, and treatment with indole-acetic acid strongly induces MtLAX2 expression in roots. mtlax2 mutants displayed root phenotypes similar to Arabidopsis aux1 mutants, including altered root gravitropism, fewer lateral roots, shorter root hairs, and auxin resistance. In addition, the activity of the synthetic DR5-GUS auxin reporter was strongly reduced in mtlax2 roots. Following inoculation with rhizobia, mtlax2 roots developed fewer nodules, had decreased DR5-GUS activity associated with infection sites, and had decreased expression of the early auxin responsive gene ARF16a Our data indicate that MtLAX2 is a functional analog of Arabidopsis AUX1 and is required for the accumulation of auxin during nodule formation in tissues underlying sites of rhizobial infection.

Highlights

  • Legume plants form a symbiotic relationship with a group of soil bacteria called rhizobia, leading to the formation of specialized root organs called nodules

  • We report that MtLAX2 plays an important role in the formation of root nodules and lateral roots in legumes, indicating common requirements for auxin influx activity for both forms of lateral organs

  • Nonsymbiotic expression of MtLAX2 was seen in root tips, lateral root primordia, and vascular tissues, matching the patterns observed for Arabidopsis AUX1 (Swarup et al, 2001; Péret et al, 2012)

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Summary

Introduction

Legume plants form a symbiotic relationship with a group of soil bacteria called rhizobia, leading to the formation of specialized root organs called nodules. Plants integrate internal developmental cues and environmental signals to regulate root growth including the production of lateral roots for anchoring in the soil and nutrient foraging One example of this is the formation of lateral roots in response to low nitrogen availability. Knockdown of several M. truncatula PLETHORA family members, encoding transcription factors that have been linked to auxin biosynthesis in Arabidopsis (Aida et al, 2004; Pinon et al, 2013; Yamaguchi et al, 2016), reduced nodulation and impaired nodule-meristem function in M. truncatula (Franssen et al, 2015) Based on these observations we can predict further overlap in the genes involved in the formation of nodules and lateral roots, but that different timing, levels, and location of expression of these genes will be important in determining which lateral organ is formed

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