Abstract
Legumes form symbiosis with rhizobia, which fix nitrogen for the benefit of host plant in return for carbon resources. Development of this unique symbiosis in legumes is triggered by rhizobia-secreted nodulation (Nod) factors (NFs). NFs, upon perception, activate Nod signaling cascade, leading to reprogramming of host cell (root) developmental networks to pave way for accommodating rhizobial symbionts. A long-cherished goal of legume-rhizobia symbiosis research is to extend this symbiotic nitrogen-fixing capacity to cereal plants such as rice. As a part of achieving this ultimate goal, in this work, initially we expressed legume-specific Nod factor receptor protein (NFRP) genes, MtNFP, MtLYK3, and LjLNP, in rice and assessed their impact on NF perception and consequently triggered biological responses in roots. RNA-seq analysis revealed that roots of both control and NFRP-expressing plants perceive NFs, but NFs elicited contrasting impacts on gene expression patterns in roots of these plants. In contrast to suppressive role of NFs on expression of several genes involved in innate immune response in roots of control plants, in NFRP-expressing plants, NFs triggered massive upregulation of a vast array of genes associated with signaling, defense response, and secondary metabolism networks in roots. Expression of NFRPs in rice also conferred root hairs the ability to respond to NFs in terms of exhibiting deformations, albeit at low levels. Together, results of the study demonstrated that rice plants have inherent ability to perceive NFs, but the expression of legume NFRPs rendered rice roots hypersensitive to NFs.
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Data Availability
All data generated from this investigation are included in the main text of the manuscript and in the Supplementary Files. The complete RNA-seq data have been deposited in NCBI’s Bioproject under identifiers PRJNA545468, GSE131964 (https://www.ncbi.nlm.nih.gov/bioproject/?term=GSE131964).
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Acknowledgments
We are grateful to Dr. PHD Schünmann (CSIRO Plant Industry, Canberra, Australia) for his kind gift of pUbi.tm1 and pWAct.GUS vectors, Dr. T Tzfira (University of Michigan, Ann Arbor, USA) for donating pSAT-RCS2-Hpt modular vector system, Dr. DJ Gage (University of Connecticut, Storrs, USA) for gifting pDG77, Dr. Luis Cárdenas (Instituto de Biotecnología, Universidad Nacional Autónoma de México) for pMP604, and Dr. WJ Broughton and Dr. X Perret (LBMPS, Universite de Geneve, Switzerland) for providing Rhizobium NGR234-Ω-nodD2 and S. rhizobium (pA28) strains. We thank Biol. Olivia Santana and Dr. Luis Cárdenas (Instituto de Biotecnología, UNAM) for advice in purification of Nod factors, Ms. Anjulata Singh (The Energy and Resources Institute, New Delhi) for the help in determining the orientations of gene expression cassettes in pPhL vector, and Dr. Jesús Arellano for guidance in particle bombardment of rice calli. This work is part of the doctoral thesis of Altúzar-Molina A. in the Programa de Doctorado en Ciencias Bioquímicas, Instituto de Biotecnología, Universidad Nacional Autónoma de México, and she gratefully acknowledges the Mexican Consejo Nacional de Ciencia y Tecnología (CONACyT) for fellowship (204969).
Funding
Financial support for the project was provided by CONACyT-Mexico (128135), DGAPA-PAPIIT-UNAM (IN206208) and DBT, India (BT/PR13634/AGIII/103/897/2015) to PM Reddy.
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AA-M performed experiments and wrote manuscript. LL carried out bioinformatic analysis. MO-B, MR, SS, and SD-R contributed in primer designing and quantitative RT-PCR experiments. LM, MLV-H, and SS-K performed Southern blot analyses. NM performed statistical analysis. GH critically reviewed the article and provided inputs. PMR conceptualized and planed the project and vector construction and contributed to manuscript writing.
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Key Message
• Extensive dissimilarities in gene expression patterns in control and NFRP-expressing rice plants in response to NFs suggest that the “putative NF receptors” of rice and the “NF receptors” of legumes transmit Nod signal differently, activating distinct signaling pathways to elicit disparate gene expression cascades in rice roots.
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Effect of expression of NFRPs and NFs on differential gene expression in rice roots (XLSX 221 kb)
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Altúzar-Molina, A., Lozano, L., Ortíz-Berrocal, M. et al. Expression of the Legume-Specific Nod Factor Receptor Proteins Alters Developmental and Immune Responses in Rice. Plant Mol Biol Rep 38, 262–281 (2020). https://doi.org/10.1007/s11105-019-01188-9
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DOI: https://doi.org/10.1007/s11105-019-01188-9