Strigolactone Biosynthesis in Medicago truncatula and Rice Requires the Symbiotic GRAS-Type Transcription Factors NSP1 and NSP2

Wei Liu,Harro J Bouwmeester,Tatsiana Charnikhova,Kerstin Kaufmann,Wei-Cai Yang,Rik Op Den Camp,Marijke Hartog,Wouter Kohlen,Erik Limpens,Guido J.E.J Hooiveld,Cezary Smaczniak,Ton Bisseling,Sergey Ivanov,Muhammad Jamil,Alessandra Lillo,René Geurts

doi:10.1105/tpc.111.089771

Abstract

Legume GRAS (GAI, RGA, SCR)-type transcription factors NODULATION SIGNALING PATHWAY1 (NSP1) and NSP2 are essential for rhizobium Nod factor-induced nodulation. Both proteins are considered to be Nod factor response factors regulating gene expression after symbiotic signaling. However, legume NSP1 and NSP2 can be functionally replaced by nonlegume orthologs, including rice (Oryza sativa) NSP1 and NSP2, indicating that both proteins are functionally conserved in higher plants. Here, we show that NSP1 and NSP2 are indispensable for strigolactone (SL) biosynthesis in the legume Medicago truncatula and in rice. Mutant nsp1 plants do not produce SLs, whereas in M. truncatula, NSP2 is essential for conversion of orobanchol into didehydro-orobanchol, which is the main SL produced by this species. The disturbed SL biosynthesis in nsp1 nsp2 mutant backgrounds correlates with reduced expression of DWARF27, a gene essential for SL biosynthesis. Rice and M. truncatula represent distinct phylogenetic lineages that split approximately 150 million years ago. Therefore, we conclude that regulation of SL biosynthesis by NSP1 and NSP2 is an ancestral function conserved in higher plants. NSP1 and NSP2 are single-copy genes in legumes, which implies that both proteins fulfill dual regulatory functions to control downstream targets after rhizobium-induced signaling as well as SL biosynthesis in nonsymbiotic conditions.

Highlights

Strigolactones (SLs) exuded by plant roots into the rhizosphere are well-known stimuli for symbiotic arbuscular mycorrhizal fungi of the order Glomeromycota (Akiyama et al, 2005)
Because NODULATION SIGNALING PATHWAY1 (NSP1) and NSP2 can act as heterodimers (Hirsch et al, 2009), we searched for genes with decreased expression in both mutants
42 probe sets fulfill this criterion. The expression of these genes was subsequently studied by quantitative (q) RT-PCR in an independent experiment that included the M. truncatula nsp1 nsp2 double mutant

Summary

Introduction

Strigolactones (SLs) exuded by plant roots into the rhizosphere are well-known stimuli for symbiotic arbuscular mycorrhizal fungi of the order Glomeromycota (Akiyama et al, 2005). These ex planta signals are coopted by root-parasitic plants of the Orobanchaceae family and are essential to induce their germination (Cook et al, 1966; Bouwmeester et al, 2007). A novel lateral root organ, the root nodule, is formed in response to specific lipo-chito-oligosaccharides secreted by the bacterium These signals, named nodulation (Nod) factors, show strong resemblance to lipo-chito-oligosaccharides produced by mycorrhizal fungi (Maillet et al, 2011).

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