Abstract
Sumoylation, ubiquitination, and phosphorylation are pivotal post-translational modifications that play key roles in regulating the homeostasis of nitrogen (N). Sumoylation comprises conjugation/deconjugation of Small Ubiquitin-like Modifier (SUMO) proteins to other proteins thereby modifying their functions. The first step in SUMO conjugation is catalyzed by the heterodimeric E1 activating enzyme. It comprises small SAE1 and large SAE2 subunits, which are encoded by three (SAE1a, SAE1b1, and SAE1b2) and one (SAE2) gene, respectively in Arabidopsis. OsSAE1a is the ortholog of Arabidopsis in rice. Here, the role of OsSAE1a in the acquisition and mobilization of N, and its influence on the growth and development of rice was investigated. The qRT-PCR assay revealed a significant increase in the relative expression level of OsSAE1a in the roots of the seedlings grown hydroponically under LN condition (0 mM NH4NO3) compared with the roots of the seedlings grown under NN (1.25 mM NH4NO3) condition for 1 day. Further, the reverse genetics approach was used by generating rice transgenic lines with RNAi-mediated knockdown of OsSAE1a. Although there was an increase in the influx of 15N-NH4+, the root/shoot ratio of RNAi lines reduced compared with the wild-type during N deficiency. N deficiency also triggered up-regulation of some of the genes (OsAMT1;2, OsAMT1;3, OsNRT2.1, OsNRT2.2, OsNRT2.3a, OsNRT2.4, and OsNAR2.2) in RNAi lines that are implicated in regulating the acquisition and/or mobilization of N. Further, RNAi lines also exhibited adverse effects on several traits (panicle length, per cent seed set, and total N concentration in the lower leaf blade) during growth to the maturity in a potting mix. The study thus highlighted the regulatory influences of OsSAE1a on the acquisition and mobilization of N, and some of the traits governing growth and development.
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Abbreviations
- AMTs:
-
Ammonium transporters
- N:
-
Nitrogen
- NH4 + :
-
Ammonium
- NO3 − :
-
Nitrate
- NUE:
-
N use efficiency
- OsSIZ1 :
-
Oryza sativa SAP (scaffold attachment factor, acinus, protein inhibitor of activated signal transducer and activator of transcription) and Miz1 (Msx2-interacting zinc finger)
- O2 :
-
Oxygen
- Pi:
-
Phosphate
- PTM:
-
Post-translational modification
- qRT-PCR:
-
Quantitative reverse transcription-PCR
- SAE:
-
SUMO-activating enzyme
- SUMO:
-
Small Ubiquitin-Like Modifier
References
Abbott A (2009) Plant genetics database at risk as funds run dry. Nature 462:258–259
Ai H, Cao Y, Jain A et al (2020) The ferroxidase LPR5 functions in the maintenance of phosphate homeostasis and is required for normal growth and development of rice. J Exp Bot 71:4828–4842
Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption by barley. Plant Physiol 99:1294–1301
Boggio R, Passafaro A, Chiocca S (2007) Targeting SUMO E1 to ubiquitin ligases: a viral strategy to counteract sumoylation. J Biol Chem 282:15376–15382
Bradstreet RB (1954) Kjeldahl method for organic nitrogen. Anal Chem 26:185–187
Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4+ cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258
Chaikam V, Karlson DT (2010) Response and transcriptional regulation of rice SUMOylation system during development and stress conditions. BMB Rep 43:103–109
Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206
Datta M, Kaushik S, Jyoti A, Mathur N, Kothari SL, Jain A (2018) SIZ1-mediated SUMOylation during phosphate homeostasis in plants: looking beyond the tip of the iceberg. Semin Cell Dev Biol 74:123–132
Dechorgnat J, Nguyen CT, Armengaud P, Jossier M, Diatloff E, Filleur S, Daniel-Vedele F (2011) From the soil to the seeds: the long journey of nitrate in plants. J Exp Bot 62:1349–1359
Ding C, Wang Y, You S, Liu Z, Wang S, Ding Y (2016) Digital gene expression analysis reveals nitrogen fertilizer increases panicle size by repressing Hd3a signaling in rice. Plant Growth Regul 79:47–54
Elrouby N (2015) Analysis of Small Ubiquitin-Like Modifier (SUMO) targets reflects the essential nature of protein SUMOylation and provides insight to elucidate the role of SUMO in plant development. Plant Physiol 169:1006–1017
Fan X, Tang Z, Tan Y, Zhang Y, Luo B, Yang M, Lian X, Shen Q, Miller AJ, Xu G (2016) Overexpression of a pH-sensitive nitrate transporter in rice increases crop yields. Proc Natl Acad Sci USA 113:7118–7123
Feng H, Yan M, Fan X, Li B, Shen Q, Miller AJ, Xu G (2011) Spatial expression and regulation of rice high-affinity nitrate transporters by nitrogen and carbon status. J Exp Bot 62:2319–2332
Ferreira LM, de Souza VM, Tavares OCH, Zonta E, Santa-Catarina C, de Souza SR, Fernandes MS, Santos LA (2015) OsAMT1.3 expression alters rice ammonium uptake kinetics and root morphology. Plant Biotechnol Rep 9:221–229
Friso G, van Wijk KJ (2015) Posttranslational protein modifications in plant metabolism. Plant Physiol 169:1469–1487
Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wirén N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. Plant Cell 11:937–947
Goff SA (1999) Rice as a model for cereal genomics. Curr Opin Plant Biol 2:86–89
Haynes RJ, Goh KM (1978) Ammonium and nitrate nutrition of plants. Biol Rev 53:465–510
Ikehashi H (2007) The origin of flooded rice cultivation. Rice Sci 14:161–171
International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Izawa T, Shimamoto K (1996) Becoming a model plant: the importance of rice to plant science. Trends Plant Sci 1:95–99
Jung KH, An G, Ronald PC (2008) Towards a better bowl of rice: assigning function to tens of thousands of rice genes. Nat Rev Genet 9:91–101
Kirk GJD, Kronzucker HJ (2005) The potential for nitrification and nitrate uptake in the rhizosphere of wetland plants: a modelling study. Ann Bot 96:639–646
Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61
Kronzucker HJ, Kirk GJD, Siddiqi MY, Glass ADM (1998) Effects of hypoxia on 13NH4+ fluxes in rice roots. Kinetics and compartmental analysis. Plant Physiol 116:581–587
Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (1999) Nitrate-ammonium synergism in rice. A subcellular flux analysis. Plant Physiol 119:1041–1045
Kronzucker HJ, Britto DT, Davenport RJ, Tester M (2001) Ammonium toxicity and the real cost of transport. Trends Plant Sci 6:335–337
Ledford H (2010) Plant biologists fear for cress project. Nature 464:154
Li YL, Fan XR, Shen QR (2008) The relationship between rhizosphere nitrification and nitrogen-use efficiency in rice plants. Plant Cell Environ 31:73–85
Li C, Tang Z, Wei J, Qu H, Xie Y, Xu G (2016) The OsAMT1.1 gene functions in ammonium uptake and ammonium-potassium homeostasis over low and high ammonium concentration ranges. J Genet Genom 43:639–649
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
López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123
Loqué D, von Wirén N (2004) Regulatory levels for the transport of ammonium in plant roots. J Exp Bot 55:1293–1305
Miura K, Hasegawa PM (2010) SUMOylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232
Näsholm T, Ekblad A, Nordin A, Giesler R, Högberg M, Högberg P (1998) Boreal forest plants take up organic nitrogen. Nature 392:914–916
Oiestad AJ, Martin JM, Giroux MJ (2019) Yield increases resulting from AGPase overexpression in rice are reliant on plant nutritional status. Plant Growth Regul 89:179–190
Park HC, Kim H, Koo SC et al (2010) Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2 in rice. Plant Cell Environ 33:1923–1934
Pearson J, Stewart GR (1993) The deposition of atmospheric ammonia and its effects on plants. New Phytol 125:283–305
Pei W, Jain A, Sun Y et al (2017) OsSIZ2 exerts regulatory influences on the developmental responses and phosphate homeostasis in rice. Sci Rep 25:12280
Pei W, Jain A, Ai H, Liu X, Feng B, Wang X, Sun Y, Xu G, Sun S (2019) OsSIZ2 regulates nitrogen homeostasis and some of the reproductive traits in rice. J Plant Physiol 232:51–60
Pei W, Jain A, Zhao B, Feng B, Xu D, Wang X (2020) Knockdown of OsSAE1a affects the growth and development and phosphate homeostasis in rice. J Plant Physiol 255:153275
Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97–125
Santamaria P, Elia A (1997) Producing nitrate-free endive heads: effect of nitrogen form on growth, yield, and ion composition of endive. J Am Soc Hortic Sci 122:140–145
Sasakawa H, Yamamoto Y (1978) Comparison of the uptake of nitrate and ammonium by rice seedlings. Plant Physiol 62:665–669
Shimamoto K, Kyozuka J (2002) Rice as a model for comparative genomics of plants. Annu Rev Plant Biol 53:399–419
Sonoda Y, Ikeda A, Saiki S, von Wirén N, Yamaya T, Yamaguchi J (2003) Distinct expression and function of three ammonium transporter genes (OsAMT1.1-1.3) in rice. Plant Cell Physiol 44:726–734
Sun Y, Jain A, Xue Y et al (2020) OsSQD1 at the crossroads of phosphate and sulfur metabolism affects plant morphology and lipid composition in response to phosphate deprivation. Plant Cell Environ 43:1669–1690
Ta TC, Ohira K (1981) Effects of various environmental and medium conditions on the response of Indica and Japonica rice plants to ammonium and nitrate nitrogen. Soil Sci Plant Nutr 27:347–355
Ta TC, Tsutsumi M, Kurihara K (1981) Comparative study on the response of Indica and Japonica rice plants to ammonium and nitrate nitrogen. Soil Sci Plant Nutr 27:83–92
Tang Z, Fan X, Li Q, Feng H, Miller AJ, Shen Q, Xu G (2012) Knockdown of a rice stelar nitrate transporter alters long-distance translocation but not root influx. Plant Physiol 160:2052–2063
Thangasamy S, Guo CL, Chuang MH, Lai MH, Chen J, Jauh GY (2011) Rice SIZ1, a SUMO E3 ligase, controls spikelet fertility through regulation of anther dehiscence. New Phytol 189:869–882
Upadhyaya NM, Surin B, Ramm K, Gaudron J, Schünmann PHD, Taylor W, Waterhouse PM, Wang MB (2000) Agrobacterium-mediated transformation of Australian rice cultivars Jarrah and Amaroo using modified promoters and selectable markers. Aust J Plant Physiol 27:201–210
Vance CP (2001) Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiol 127:390–397
Wang MY, Siddiqi MY, Ruth TJ, Glass ADM (1993) Ammonium uptake by rice roots. I. Fluxes and subcellular distribution of 13NH4+. Plant Physiol 103:1249–1258
Wang H, Makeen K, Yan Y, Cao Y, Sun S, Xu G (2011) OsSIZ1 regulates the vegetative growth and reproductive development in rice. Plant Mol Biol Rep 29:411–417
Wang H, Sun R, Cao Y et al (2015) OsSIZ1, a SUMO E3 ligase gene, is involved in the regulation of the responses to phosphate and nitrogen in rice. Plant Cell Physiol 56:2381–2395
Wang JJ, Li Z, Jin X, Liang G, Struik PC, Gu J, Zhou Y (2019) Phenotyping flag leaf nitrogen content in rice using a three-band spectral index. Comput Electron Agric 162:475–481
Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182
Yan M, Fan X, Feng H, Miller AJ, Shen Q, Xu G (2011) Rice OsNAR2.1 interacts with OsNRT2.1, OsNRT2.2 and OsNRT2.3a nitrate transporters to provide uptake over high and low concentration ranges. Plant Cell Environ 34:1360–1372
Yan C, Chen H, Fan T, Huang Y, Yu S, Chen S, Hong X (2012) Rice flag leaf physiology, organ and canopy temperature in response to water stress. Plant Prod Sci 15:92–99
Yang S, Hao D, Cong Y, Jin M, Su Y (2015) The rice OsAMT1;1 is a proton-independent feedback regulated ammonium transporter. Plant Cell Rep 34:321–330
Zhang X, Lei J, Zheng D, Liu Z, Li G, Wang S, Ding Y (2017) Amino acid composition of leaf, grain and bracts of japonica rice (Oryza Sativa ssp. Japonica) and its response to nitrogen fertilization. Plant Growth Regul 82:1–9
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This work was supported by Chinese National Natural Science Foundation (31672226).
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SS and XW developed the ideas, designed and supervised all the experiments. Experiments and analyses were performed by XW, WP, ZH and XH, AJ and XW prepared the final manuscript.
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Wang, X., Jain, A., Pei, W. et al. Knockdown of OsSAE1a affects acquisition and mobilization of nitrogen, and growth and development of rice. Plant Growth Regul 94, 221–231 (2021). https://doi.org/10.1007/s10725-021-00706-8
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DOI: https://doi.org/10.1007/s10725-021-00706-8