Abstract
Main conclusion
Rpf107 is involved in the infection process of rhizobia and the maintenance of symbiotic nitrogen fixation in black locust root nodules.
Abstract
The LURP-one related (LOR) protein family plays a pivotal role in mediating plant defense responses against both biotic and abiotic stresses. However, our understanding of its function in the symbiotic interaction between legumes and rhizobia remains limited. Here, Rpf107, a homolog of LOR, was identified in Robinia pseudoacacia (black locust). The subcellular localization of Rpf107 was analyzed, and its function was investigated using RNA interference (RNAi) and overexpression techniques. The subcellular localization assay revealed that Rpf107 was mainly distributed in the plasma membrane and nucleus. Rpf107 silencing prevented rhizobial infection and hampered plant growth. The number of infected cells in the nitrogen fixation zone of the Rpf107-RNAi nodules was also noticeably lower than that in the control nodules. Notably, Rpf107 silencing resulted in bacteroid degradation and the premature aging of nodules. In contrast, the overexpression of Rpf107 delayed the senescence of nodules and prolonged the nitrogen-fixing ability of nodules. These results demonstrate that Rpf107 was involved in the infection of rhizobia and the maintenance of symbiotic nitrogen fixation in black locust root nodules. The findings reveal that a member of the LOR protein family plays a role in leguminous root nodule symbiosis, which is helpful to clarify the functions of plant LOR protein family and fully understand the molecular mechanisms underlying legume–rhizobium symbiosis.
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Data availability
The Rpf107 gene sequence data generated in this study are available in GenBank of the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/nuccore) under the access numbers: JK974217.
Abbreviations
- dpi:
-
Days post-inoculation
- GFP:
-
Green fluorescent protein
- Hpa :
-
Hyaloperonospora arabidopsidis
- ITs:
-
Infection threads
- Lb :
-
Leghemoglobin gene
- LOR:
-
LURP-one related
- LURP1 :
-
Late upregulated in response to Hpa
- PLSCR:
-
Phospholipid scramblase
- R :
-
Plant disease resistance genes
- RNAi:
-
RNA interference
- TEM:
-
Transmission electron microscopy
References
Alesandrini F, Mathis R, Van de Sype G, Hérouart D, Puppo A (2003) Possible roles for a cysteine protease and hydrogen peroxide in soybean nodule development and senescence. New Phytol 158:131–138
Bag S, Mondal A, Majumder A, Mondal SK, Banik A (2022) Flavonoid mediated selective cross-talk between plants and beneficial soil microbiome. Phytochem Rev 21:1739–1760
Baig A (2018) Role of Arabidopsis LOR1 (LURP-one related one) in basal defense against Hyaloperonospora arabidopsidis. Physiol Mol Plant Pathol 103:71–77
Bateman A, Finn RD, Sims PJ, Wiedmer T, Biegert A, Söding J (2009) Phospholipid scramblases and Tubby-like proteins belong to a new superfamily of membrane tethered transcription factors. Bioinformatics 25:159–162
Ben-Efraim I, Zhou Q, Wiedmer T, Gerace L, Sims PJ (2004) Phospholipid scramblase 1 is imported into the nucleus by a receptor-mediated pathway and interacts with DNA. Biochemistry 43:3518–3526
Bensmihen S (2015) Hormonal control of lateral root and nodule development in legumes. Plants 4:523–547
Boggon TJ, Shan W, Santagata S, Myers SC, Shapiro L (1999) Implication of tubby proteins as transcription factors by structure-based functional analysis. Science 286:2119–2125
Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant-Microbe Interact 14:695–700
Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406
Brechenmacher L, Kim M, Benitez M, Li M, Joshi T, Calla B, Lee MP, Libault M, Vodkin LO, Xu D (2008) Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol Plant-Microbe Interact 21:631–645
Cabeza R, Koester B, Liese R, Lingner A, Baumgarten V, Dirks J, Salinas-Riester G, Pommerenke C, Dittert K, Schulze J (2014) An RNA sequencing transcriptome analysis reveals novel insights into molecular aspects of the nitrate impact on the nodule activity of Medicago truncatula. Plant Physiol 164:400–411
Cao Y, Halane MK, Gassmann W, Stacey G (2017) The role of plant innate immunity in the legume-rhizobium symbiosis. Annu Rev Plant Biol 68:535–561
Capoen W, Goormachtig S, De Rycke R, Schroeyers K, Holsters M (2005) SrSymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci USA 102:10369–10374
Chen Y, Hui H, Yang H, Zhao K, Qin Y, Gu C, Wang X, Lu N, Guo Q (2013) Wogonoside induces cell cycle arrest and differentiation by affecting expression and subcellular localization of PLSCR1 in AML cells. Blood 121:3682–3691
Chungopast S, Hirakawa H, Sato S, Handa Y, Saito K, Kawaguchi M, Tajima S, Nomura M (2014) Transcriptomic profiles of nodule senescence in Lotus japonicus and Mesorhizobium loti symbiosis. Plant Biotechnol-Nar 31:345–349
Cilliers M, van Wyk SG, van Heerden PDR, Kunert KJ, Vorster BJ (2018) Identification and changes of the drought-induced cysteine protease transcriptome in soybean (Glycine max) root nodules. Environ Exp Bot 148:59–69
Clúa J, Roda C, Zanetti ME, Blanco FA (2018) Compatibility between legumes and rhizobia for the establishment of a successful nitrogen-fixing symbiosis. Genes 9:125
Coates ME, Beynon JL (2010) Hyaloperonospora arabidopsidis as a pathogen model. Annu Rev Phytopathol 48:329–345
Coker TLR, Cevik V, Beynon JL, Gifford ML (2015) Spatial dissection of the Arabidopsis thaliana transcriptional response to downy mildew using fluorescence activated cell sorting. Front Plant Sci 6:527
Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511
Dal Col J, Lamberti MJ, Nigro A, Casolaro V, Fratta E, Steffan A, Montico B (2022) Phospholipid scramblase 1: a protein with multiple functions via multiple molecular interactors. Cell Commun Signal 20:1–15
Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833
Deakin WJ, Broughton WJ (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat Rev Microbiol 7:312–320
El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler A, Becker A, Gouzy J, Vernié T, Gough C, Niebel A (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136:3159–3176
Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371
Fåhraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. Microbiology 16:374–381
Fan M, Liu Z, Nan L, Wang E, Chen W, Lin Y, Wei G (2018) Isolation, characterization, and selection of heavy metal-resistant and plant growth-promoting endophytic bacteria from root nodules of Robinia pseudoacacia in a Pb/Zn mining area. Microbiol Res 217:51–59
Fang Y, Cao D, Yang H, Guo W, Ouyang W, Chen H, Shan Z, Yang Z, Chen S, Li X (2021) Genome-wide identification and characterization of soybean GmLOR gene family and expression analysis in response to abiotic stresses. Int J Mol Sci 22:12515
Gavrin A, Kaiser BN, Geiger D, Tyerman SD, Wen Z, Bisseling T, Fedorova EE (2014) Adjustment of host cells for accommodation of symbiotic bacteria: vacuole defunctionalization, HOPS suppression, and TIP1g retargeting in Medicago. Plant Cell 26:3809–3822
Gourion B, Berrabah F, Ratet P, Stacey G (2015) Rhizobium-legume symbioses: the crucial role of plant immunity. Trends Plant Sci 20:186–194
Holub EB (2008) Natural history of Arabidopsis thaliana and oomycete symbioses. Eur J Plant Pathol 122:91–109
Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329
Kardailsky IV, Brewin NJ (1996) Expression of cysteine protease genes in pea nodule development and senescence. Mol Plant-Microbe Interact 9:689–695
Katagiri F (2004) A global view of defense gene expression regulation-a highly interconnected signaling network. Curr Opin Plant Biol 7:506–511
Knoth C, Eulgem T (2008) The oomycete response gene LURP1 is required for defense against Hyaloperonospora parasitica in Arabidopsis thaliana. Plant J 55:53–64
Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant-Microbe Interact 20:120–128
Kouchi H, Shimomura K, Hata S, Hirota A, Wu G, Kumagai H, Tajima S, Suganuma N, Suzuki A, Aoki T (2004) Large-scale analysis of gene expression profiles during early stages of root nodule formation in a model legume, Lotus japonicus. DNA Res 11:263–274
Kusano S, Ikeda M (2019) Interaction of phospholipid scramblase 1 with the Epstein-Barr virus protein BZLF1 represses BZLF1-mediated lytic gene transcription. J Biol Chem 294:15104–15116
Lee MH, Jeon HS, Kim HG, Park OK (2017) An Arabidopsis NAC transcription factor NAC4 promotes pathogen-induced cell death under negative regulation by microRNA164. New Phytol 214:343–360
Li M, Xu J, Wang X, Fu H, Zhao M, Wang H, Shi L (2018) Photosynthetic characteristics and metabolic analyses of two soybean genotypes revealed adaptive strategies to low-nitrogen stress. J Plant Physiol 229:132–141
Liesebach H, Schneck V (2017) Chloroplast DNA variation in planted and natural regenerated stands of black locust (Robinia pseudoacacia L.). Silvae Genet 61:27–35
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2- ΔΔCT method. Methods 25:402–408
Lohar DP, Sharopova N, Endre G, Penuela S, Samac D, Town C, Silverstein KA, VandenBosch KA (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 140:221–234
Lu N, Dai L, Wu B, Zhang Y, Luo Z, Xun S, Sun Y, Li Y (2015) A preliminary study on the crossability in Robinia pseudoacacia L. Euphytica 206:555–566
Luo W, Zhang J, Liang L, Wang G, Li Q, Zhu P, Zhou Y, Li J, Zhao Y, Sun N (2018) Phospholipid scramblase 1 interacts with influenza a virus NP, impairing its nuclear import and thereby suppressing virus replication. Plos Pathog 14:e1006851
Macho AP, Zipfel C (2014) Plant PRRs and the activation of innate immune signaling. Mol Cell 54:263–272
Martin-Sampedro R, Santos JI, Eugenio ME, Wicklein B, Jimenez-Lopez L, Ibarra D (2019) Chemical and thermal analysis of lignin streams from Robinia pseudoacacia L. generated during organosolv and acid hydrolysis pre-treatments and subsequent enzymatic hydrolysis. Int J Biol Macromol 140:311–322
Mbengue MD, Hervé C, Debellé F (2020) Nod factor signaling in symbiotic nodulation. Adv Bot Res 94:1–39
Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset A, Barloy-Hubler F, Galibert F, Kondorosi A (2006) Eukaryotic control on bacterial cell cycle and differentiation in the rhizobium-legume symbiosis. Proc Natl Acad Sci USA 103:5230–5235
Mohamad OA, Hao X, **e P, Hatab S, Lin Y, Wei G (2012) Biosorption of copper (II) from aqueous solution using non-living Mesorhizobium amorphae strain CCNWGS0123. Microbes Environ 27:234–241
Monahan-Giovanelli H, Pinedo CA, Gage DJ (2006) Architecture of infection thread networks in develo** root nodules induced by the symbiotic bacterium Sinorhizobium meliloti on Medicago truncatula. Plant Physiol 140:661–670
Naito Y, Fujie M, Usami S, Murooka Y, Yamada T (2000) The involvement of a cysteine proteinase in the nodule development in Chinese milk vetch infected with Mesorhizobium huakuii subsp. rengei. Plant Physiol 124:1087–1096
Nawaz MA, Han X, Chen C, Zheng Z, Shireen F, Bie Z, Huang Y (2018) Nitrogen use efficiency of watermelon grafted onto 10 wild watermelon rootstocks under low nitrogen conditions. Agronomy 8:259
Okazaki S, Kaneko T, Sato S, Saeki K (2013) Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc Natl Acad Sci USA 110:17131–17136
Palanirajan SK, Gummadi SN (2019) Heavy-metals-mediated phospholipids scrambling by human phospholipid scramblase 3: a probable role in mitochondrial apoptosis. Chem Res Toxicol 33:553–564
Papaioannou A, Chatzistathis T, Papaioannou E, Papadopoulos G (2016) Robinia pseudοacacia as a valuable invasive species for the restoration of degraded croplands. CATENA 137:310–317
Patra JK, Kim ES, Oh K, Kim H, Dhakal R, Kim Y, Baek K (2015) Bactericidal effect of extracts and metabolites of Robinia pseudoacacia L. on Streptococcus mutans and Porphyromonas gingivalis causing dental plaque and periodontal inflammatory diseases. Molecules 20:6128–6139
Pérez Guerra JC, Coussens G, De Keyser A, De Rycke R, De Bodt S, Van De Velde W, Goormachtig S, Holsters M (2010) Comparison of developmental and stress-induced nodule senescence in Medicago truncatula. Plant Physiol 152:1574–1584
Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201
Pierre O, Hopkins J, Combier M, Baldacci F, Engler G, Brouquisse R, Hérouart D, Boncompagni E (2014) Involvement of papain and legumain proteinase in the senescence process of Medicago truncatula nodules. New Phytol 202:849–863
Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J (2012) The Pfam protein families database. Nucleic Acids Res 40:D290–D301
Puppo A, Groten K, Bastian F, Carzaniga R, Soussi M, Lucas MM, De Felipe MR, Harrison J, Vanacker H, Foyer CH (2005) Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol 165:683–701
Qin J, ** W, Rahmlow A, Kong H, Zhang Z, Shangguan Z (2016) Effects of forest plantation types on leaf traits of Ulmus pumila and Robinia pseudoacacia on the Loess Plateau, China. Ecol Eng 97:416–425
Rosu AF, Bita A, Calina D, Rosu L, Zlatian O, Calina V (2012) Synergic antifungal and antibacterial activity of alcoholic extract of the species Robinia pseudoacacia L. (Fabaceae). Eur J Hosp Pharm 19:216
Saengwilai P, Tian X, Lynch JP (2014) Low crown root number enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol 166:581–589
Seabra AR, Pereira PA, Becker JD, Carvalho HG (2012) Inhibition of glutamine synthetase by phosphinothricin leads to transcriptome reprograming in root nodules of Medicago truncatula. Mol Plant-Microbe Interact 25:976–992
Sivagnanam U, Palanirajan SK, Gummadi SN (2017) The role of human phospholipid scramblases in apoptosis: an overview. BBA-Mol Cell Res 1864:2261–2271
Tao Y, **e Z, Chen W, Glazebrook J, Chang H, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330
Van de Velde W, Guerra JCP, Keyser AD, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S (2006) Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiol 141:711–720
Vasse J, De Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306
Wais RJ, Keating DH, Long SR (2002) Structure-function analysis of nod factor-induced root hair calcium spiking in Rhizobium-legume symbiosis. Plant Physiol 129:211–224
Wang D, Yang S, Tang F, Zhu H (2012) Symbiosis specificity in the legume-rhizobial mutualism. Cell Microbiol 14:334–342
Wang X, Huo H, Luo Y, Liu D, Zhao L, Zong L, Chou M, Chen J, Wei G (2019) Type III secretion systems impact Mesorhizobium amorphae CCNWGS0123 compatibility with Robinia pseudoacacia. Tree Physiol 39:1533–1550
Wei G, Chen W, Zhu W, Chen C, Young JPW, Bontemps C (2009) Invasive Robinia pseudoacacia in China is nodulated by Mesorhizobium and Sinorhizobium species that share similar nodulation genes with native American symbionts. FEMS Microbiol Ecol 68:320–328
White J, Prell J, James EK, Poole P (2007) Nutrient sharing between symbionts. Plant Physiol 144:604–614
Wiedmer T, Zhao J, Nanjundan M, Sims PJ (2003) Palmitoylation of phospholipid scramblase 1 controls its distribution between nucleus and plasma membrane. Biochemistry 42:1227–1233
**ao TT, Schilderink S, Moling S, Deinum EE, Kondorosi E, Franssen H, Kulikova O, Niebel A, Bisseling T (2014) Fate map of Medicago truncatula root nodules. Development 141:3517–3528
Xu S, Zhu X, Li C, Ye Q (2014) Effects of CO2 enrichment on photosynthesis and growth in Gerbera jamesonii. Sci Hortic 177:77–84
Yang S, Tang F, Gao M, Krishnan HB, Zhu H (2010) R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc Natl Acad Sci USA 107:18735–18740
Zhou Q, Ben-Efraim I, Bigcas J, Junqueira D, Wiedmer T, Sims PJ (2005) Phospholipid scramblase 1 binds to the promoter region of the inositol 1, 4, 5-triphosphate receptor type 1 gene to enhance its expression. J Biol Chem 280:35062–35068
Zhu Y, Wang Y, Chen L (2019) Responses of ground-active arthropods to black locust (Robinia pseudoacacia L.) afforestation in the Loess Plateau of China. CATENA 183:104233
Acknowledgements
This work was supported by National Natural Science Foundation of China (No. 41977052), and Key Research & Development program of Shaanxi Province (No. 2020ZDLNY07-09).
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YLL analyzed the data and wrote the paper. YLL,YYW, ZYY, RS, LZ, and ZF conducted the experiments and collected data. MXC designed the research and reviewed and edited the manuscript. GHW provided an experimental platform. All authors read and approved the final manuscript.
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Li, Y., Wu, Y., Yang, Z. et al. The Rpf107 gene, a homolog of LOR, is required for the symbiotic nodulation of Robinia pseudoacacia. Planta 259, 6 (2024). https://doi.org/10.1007/s00425-023-04280-3
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DOI: https://doi.org/10.1007/s00425-023-04280-3