Shoot-to-root translocated GmNN1/FT2a triggers nodulation and regulates soybean nitrogen nutrition

Abstract

Symbiotic nitrogen fixation (SNF) provides sufficient nitrogen (N) to meet most legume nutrition demands. In return, host plants feed symbionts carbohydrates produced in shoots. However, the molecular dialogue between shoots and symbionts remains largely mysterious. Here, we report the map-based cloning and characterization of a natural variation in GmNN1, the ortholog of Arabidopsis thaliana FLOWERING LOCUS T (FT2a) that simultaneously triggers nodulation in soybean and modulates leaf N nutrition. A 43-bp insertion in the promoter region of GmNN1/FT2a significantly decreased its transcription level and yielded N deficiency phenotypes. Manipulating GmNN1/GmFT2a significantly enhanced soybean nodulation, plant growth, and N nutrition. The near-isogenic lines (NILs) carrying low mRNA abundance alleles of GmNN1/FT2a, along with stable transgenic soybeans with CRISPR/Cas9 knockouts of GmNN1/FT2a, had yellower leaves, lower N concentrations, and fewer nodules than wild-type control plants. Grafting together with split-root experiments demonstrated that only shoot GmNN1/FT2a was responsible for regulating nodulation and thereby N nutrition through shoot-to-root translocation, and this process depends on rhizobial infection. After translocating into roots, shoot-derived GmNN1/FT2a was found to interact with GmNFYA-C (nuclear factor-Y subunit A-C) to activate symbiotic signaling through the previously reported GmNFYA-C-ENOD40 module. In short, the description of the critical soybean nodulation regulatory pathway outlined herein sheds novel insights into the shoot-to-root signaling required for communications between host plants and root nodulating symbionts.

Flowering time: From physiology, through genetics to mechanism

“…Along with 2 other SD-activated transmissible FT-like proteins, StSP3D and FT-like 1 (StFTL1), SP6A protein is then transported via phloem from leaves to stolons, where it forms a floral activation-like complex, termed the tuberigen activation complex, which promotes tuber formation ( Teo et al 2017 ; Jing et al 2023 ). A similar shoot-to-root translocation is found in soybean ( Glycine max ), where the shoot-derived ortholog of Arabidopsis FT, GmNN1/FT2a, triggers nodulation upon rhizobial infection ( Kong et al 2010 ; Sun et al 2011 ; Li et al 2022b ). In the root, GmNN1/FT2a interacts with GmNFYA-C to activate symbiotic signaling through the GmNFYA-C-ENOD40 module ( Li et al 2022b ).…”

Auxin regulation on crop: from mechanisms to opportunities in soybean breeding

“…Recent studies on Cryptochrome 1(CRY1)-dependent light signaling highlights the promotional effect of light signaling in shoot for soybean root nodulation. The mobile transcriptional factors TGACG-motif binding factor 3/4 (GmSTF3/4) and FLOWERING LOCUS T (GmFTs), which move from shoots to roots, activate nodulation events including upregulation of GmNIN, nuclear factor Y (GmNF-YA1 and NF-YB1) and GmENOD40 transcripts (Wang et al 2021;Li et al 2022b). Soybean GmSTFs are orthologs of Arabidopsis HY5, which has been well characterized as a central regulator of light signaling, directly or indirectly controls auxin transport and auxin signaling on transcriptional level (Cluis et al 2004;Sibout et al 2006;van Gelderen et al 2018).…”

Origin, variation, and selection of natural alleles controlling flowering and adaptation in wild and cultivated soybean

“…COL1a enhances salt and drought resistance by promoting the accumulation of DELTA1-PYRROLINE-5-CARBOXYLATE SYNTHASE (P5CS), a major player in proline biosynthesis that functions in osmoregulation (Xu et al 2023 ). Moreover, FT2a in aboveground tissue is a key factor determining the formation of soybean nodules (Li et al 2022 ). FT2a moves from shoots to roots and activates the expression of the key nodule gene EARLY NODULIN 40 ( ENOD40 ) together with the transcription factor Nuclear Factor Y (NY-F) A-C, which is specifically responsive to low nitrogen levels, thereby inducing nodule formation and improving nitrogen use efficiency in soybean (Li et al 2022 ; Wang et al 2021b ).…”

“…Moreover, FT2a in aboveground tissue is a key factor determining the formation of soybean nodules (Li et al 2022 ). FT2a moves from shoots to roots and activates the expression of the key nodule gene EARLY NODULIN 40 ( ENOD40 ) together with the transcription factor Nuclear Factor Y (NY-F) A-C, which is specifically responsive to low nitrogen levels, thereby inducing nodule formation and improving nitrogen use efficiency in soybean (Li et al 2022 ; Wang et al 2021b ). Further investigations of photoperiod-regulated plant growth and development and stress tolerance will help us to understand the molecular mechanisms underlying the plant photoperiod responses.…”