Involvement of a truncated MADS-box transcription factor ZmTMM1 in root nitrate foraging

Ying Liu,Fanjun Chen,Xuelian Li,Brian Forde,Guohua Mi,Zhongtao Jia,Zhangkui Wang,Hideki Takahashi,Lixing Yuan,Miriam Gifford

doi:10.1093/jxb/eraa116

Abstract

Plants can develop root systems with distinct anatomical features and morphological plasticity to forage nutrients distributed heterogeneously in soils. Lateral root proliferation is a typical nutrient-foraging response to a local supply of nitrate, which has been investigated across many plant species. However, the underlying mechanism in maize roots remains largely unknown. Here, we report on identification of a maize truncated MIKC-type MADS-box transcription factor (ZmTMM1) lacking K- and C-domains, expressed preferentially in the lateral root branching zone and induced by the localized supply of nitrate. ZmTMM1 belongs to the AGL17-like MADS-box transcription factor family that contains orthologs of ANR1, a key regulator for root nitrate foraging in Arabidopsis. Ectopic overexpression of ZmTMM1 recovers the defective growth of lateral roots in the Arabidopsis anr1 agl21 double mutant. The local activation of glucocorticoid receptor fusion proteins for ZmTMM1 and an artificially truncated form of AtANR1 without the K- and C-domains stimulates the lateral root growth of the Arabidopsis anr1 agl21 mutant, providing evidence that ZmTMM1 encodes a functional MADS-box that modulates lateral root development. However, no phenotype was observed in ZmTMM1-RNAi transgenic maize lines, suggesting a possible genetic redundancy of ZmTMM1 with other AGL17-like genes in maize. A comparative genome analysis further suggests that a nitrate-inducible transcriptional regulation is probably conserved in both truncated and non-truncated forms of ZmTMM1-like MADS-box transcription factors found in grass species.

Highlights

Natural and agricultural soils present a large spatial and temporal diversity in nutrient distribution (Giehl and von Wirén, 2014)
By evaluating transcript expression levels in the split-root system, OsMADS57 and ZmTMM1 were shown to be up-regulated by local nitrate supply among all the AGL17-like genes in rice and maize (Fig. 8A,B).,we propose the local nitrate-inducible expression as a conserved feature of the ZmTMM1-like genes in grass species.In contrast, all the AGL17-like genes in Arabidopsis were not regulated by local nitrate supply at the transcriptional level (Supplementary Fig. S9), suggesting that nitrate regulates AGL17-like genes via distinct mechanisms between dicots and monocots
We identified a truncated MIKC-type MADS-box transcription factor gene ZmTMM1 involved in root nitrate-foraging responses

Summary

Introduction

Natural and agricultural soils present a large spatial and temporal diversity in nutrient distribution (Giehl and von Wirén, 2014). As the main inorganic nitrogen source in aerobic soils, is heterogeneously distributed due to its high solubility and rapid mobility in soil solution (Lark et al, 2004; Miller et al, 2007).To capture the unevenly distributed nitrate, plants stimulate lateral root (LR) growth in nitrate-rich patches, which has been reported as a typical nutrient-foraging response in 4548 | Liu et al. Lines of experimental evidence suggest that nitrate per se supplied locally to roots acts as a signaling molecule to modulate LR growth (Zhang and Forde, 1998; Remans et al, 2006; Ho et al, 2009; Bouguyon et al, 2015). In Arabidopsis, local nitrate is sensed by the nitrate transceptor NRT1.1/NPF6.3, which triggers the signaling pathway involving the MADS-box transcription factor ANR1 to stimulate LR proliferation in a nitrate-enriched zone (Zhang and Forde, 1998; Remans et al, 2006; Bouguyon et al, 2015). Local nitrate can inhibit NRT1.1-facilitated auxin redistribution in LR primordia, allowing auxin accumulation for LR emergence and elongation (Krouk et al, 2010; Mounier et al, 2014)

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Conclusion