Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus.

Li Xue,Pierre-Marc Delaux,Marcel Bucher,Stefanie Junkermann,Vinod Vijayakumar,Haitao Cui,Benjamin Buer

doi:10.1104/pp.114.255430

Abstract

Arbuscular mycorrhizal (AM) fungi, in symbiosis with plants, facilitate acquisition of nutrients from the soil to their host. After penetration, intracellular hyphae form fine-branched structures in cortical cells termed arbuscules, representing the major site where bidirectional nutrient exchange takes place between the host plant and fungus. Transcriptional mechanisms underlying this cellular reprogramming are still poorly understood. GRAS proteins are an important family of transcriptional regulators in plants, named after the first three members: GIBBERELLIC ACID-INSENSITIVE, REPRESSOR of GAI, and SCARECROW. Here, we show that among 45 transcription factors up-regulated in mycorrhizal roots of the legume Lotus japonicus, expression of a unique GRAS protein particularly increases in arbuscule-containing cells under low phosphate conditions and displays a phylogenetic pattern characteristic of symbiotic genes. Allelic rad1 mutants display a strongly reduced number of arbuscules, which undergo accelerated degeneration. In further studies, two RAD1-interacting proteins were identified. One of them is the closest homolog of Medicago truncatula, REDUCED ARBUSCULAR MYCORRHIZATION1 (RAM1), which was reported to regulate a glycerol-3-phosphate acyl transferase that promotes cutin biosynthesis to enhance hyphopodia formation. As in M. truncatula, the L. japonicus ram1 mutant lines show compromised AM colonization and stunted arbuscules. Our findings provide, to our knowledge, new insight into the transcriptional program underlying the host's response to AM colonization and propose a function of GRAS transcription factors including RAD1 and RAM1 during arbuscule development.

Highlights

Arbuscular mycorrhizal (AM) fungi, in symbiosis with plants, facilitate acquisition of nutrients from the soil to their host
45 genes encoding transcription factors or transcriptional regulators were significantly up-regulated by R. irregularis compared with nonmycorrhizal roots grown in a similar low-Pi environment (Fig. 1A; Supplemental Table S1)
These genes encoded GRAS (18 members), APETALA2 (AP2)/ETHYLENE RESPONSE FACTOR (ERF; eight), NO APICAL MERISTEM, ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR and CUP-SHAPED COTYLEDON (NAC)-domain family members, MYELOBLASTOSIS (MYB; three), C2H2 zinc finger, MADS DNA-binding domain (MADS [from MINICHROMOSOME MAINTENANCE1, AGAMOUS, DEFICIENS and SERUM RESPONSE FACTOR]; two), BASIC LEUCINE ZIPPER, AUXIN RESPONSE FACTOR (ARF; one), WRKY DNA binding domain, NODULE INCEPTION (NIN)-LIKE protein, and LATERAL ORGAN BOUNDARIES (LOB) domain transcription factors, indicating the complexity of transcriptional regulation of AM symbiosis (AMS). They are distinguishable in four general expression patterns: genes that were overall highly expressed (11), genes that were only responsive to AM under low-phosphorus conditions (23), genes with high expression under low Pi regardless of AM status, and the rest of intermediate status

Summary

Introduction

Arbuscular mycorrhizal (AM) fungi, in symbiosis with plants, facilitate acquisition of nutrients from the soil to their host. We show that among 45 transcription factors up-regulated in mycorrhizal roots of the legume Lotus japonicus, expression of a unique GRAS protein increases in arbuscule-containing cells under low phosphate conditions and displays a phylogenetic pattern characteristic of symbiotic genes. NSP2 interacts with GRAS transcription factor REDUCED ARBUSCULAR MYCORRHIZATION1 (RAM1) to induce RAM2, encoding a glycerol-3-phosphate acyl transferase (GPAT), to facilitate hyphopodia formation on the root surface during mycorrhizal colonization (Gobbato et al, 2012). DELLA interacting protein (DIP1) was identified in rice, and RAM1 was shown to interact with DIP1 (Yu et al, 2014) This suggests that formation of multicomponent GRAS transcription factor complexes is a prerequisite for elicitation of nodulation or mycorrhization (Oldroyd, 2013)

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Conclusion