Abstract
Background
Excessive application of N fertilizer can inhibit plant growth, reduce N-use efficiency (NUE) and lead to production reduction. Watermelon is an important crop that often restricted by inappropriate N supply. The study aims to test whether grafting with bottle gourd rootstock can improve the NUE and growth performance of watermelon under reduced nitrate application and to clarify the underlying mechanism.
Methods
Grafted (self-grafted and rootstock-grafted watermelon) and ungrafted (watermelon and bottle gourd) seedlings were treated separately with 9 mM (control) and 4 mM (reduced-nitrate) N concentrations for 18 days under hydroponic conditions.
Results
The growth and NUE of bottle gourd rootstock-grafted watermelon seedlings increased under reduced-nitrate, while decreased slightly in self-grafted seedlings compared with the control. Rootstock-grafted plants had higher root morphological traits, NO3− accumulation, NR and GS activities, photosynthesis, and NUE traits than self-grafted plants under reduced-nitrate. Reduced-nitrate treatment significantly up-regulated the expression of nitrate transporter genes NRT1.5 and NRT2.1 and N metabolizing enzyme genes NR2, NR3, NiR, GS1 and GS2 in rootstock-grafted plants.
Conclusion
Under reduced-nitrate treatment, grafted watermelon can make better use of the developed rootstock roots to increase the NO3− absorption and transportation to the shoot, so as to enhance the N metabolism potential and photosynthetic capacity of scions, and finally improve plant growth and NUE. The enhanced NO3− uptake and utilization of rootstock-grafted plants were regulated at the transcriptional level. Grafting with the bottle gourd rootstock may be beneficial to the efficient production of watermelon and economic application of N fertilizer.
Similar content being viewed by others
Data availability
The datasets generated during and analysed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- GOGAT:
-
Glutamate synthase
- GS:
-
Glutamine synthetase
- N:
-
Nitrogen
- NA:
-
N accumulation
- NiR:
-
Nitrite reductase
- NR:
-
Nitrate reductase
- NRTs:
-
Nitrate transporters
- NUE:
-
N-use efficiency
- NUpE:
-
N uptake efficiency
- NUtE:
-
N utilization efficiency
References
Albacete A, Martínez-Andújar C, Martínez-Pérez A, Thompson AJ, Dodd IC, Pérez-Alfocea F (2015) Unravelling rootstock × scion interactions to improve food security. J Exp Bot 66:2211–2226
Allègre A, Silvestre J, Morard P, Kallerhoff J, Pinelli E (2004) Nitrate reductase regulation in tomato roots by exogenous nitrate: a possible role in tolerance to long-term root anoxia. J Exp Bot 55:2625–2634
Andrews M, Raven JA, Lea PJ (2013) Do plants need nitrate? The mechanisms by which nitrogen form affects plants. Ann Appl Biol 163:174–199
Bremner JM, Black CA, Evans DD, White IL, Ensminger LE, Clark FE (1965) Total nitrogen. Methods of soil analysis. American Society of Agronomy, Wisconsin, pp 1149–1178
Bucher CA, Santos LA, de Matos NE, Rangel RP, de Souza SR, Fernandes MS (2014) The transcription of nitrate transporters in upland rice varieties with contrasting nitrate-uptake kinetics. J Plant Nutr Soil Sci 177:395–403
Chen ZC, Ma JF (2015) Improving nitrogen use efficiency in rice through enhancing root nitrate uptake mediated by a nitrate transporter, NRT1.1B. J Genet Genomics 42:463–465
Chen HH, Jia YM, Xu H, Wang YW, Zhou Y, Huang ZR, Yang LT, Li Y, Chen LS, Guo JX (2020) Ammonium nutrition inhibits plant growth and nitrogen uptake in citrus seedlings. Sci Hortic 272:109526
Colla G, Rouphael Y, Mirabelli C, Cardarelli M (2011) Nitrogen-use efficiency traits of mini-watermelon in response to grafting and nitrogen fertilization doses. J Plant Nutr Soil Sci 174:933–941
De Oliveira MMT, Lu SH, Zurgil U, Raveh E, Tel-Zur N (2021) Grafting in Hylocereus (Cactaceae) as a tool for strengthening tolerance to high temperature stress. Plant Physiol Biochem 160:94–105
Dordas C (2017) Nitrogen nutrition index and leaf chlorophyll concentration and its relationship with nitrogen use efficiency in barley (Hordeum vulgare L.). J Plant Nutr 40:1190–1203
Elliott GC, Läuchli A (1985) Phosphorus efficiency and phosphate-iron interaction in maize. Agron J 77:399–403
Fullana-Pericàs M, Conesa MÀ, Pérez-Alfocea F, Galmés J (2020) The influence of grafting on crops’ photosynthetic performance. Plant Sci 295:110250
Garnett T, Plett D, Conn V, Conn S, Rabie H, Rafalski JA, Dhugga K, Tester MA, Kaiser BN (2015) Variation for N uptake system in maize: genotypic response to N supply. Front Plant Sci 6:936
Gomes LDL, Ferreira ML, Kanashiro S, Tavares AR (2021) Nitrogen uptake by ornamental bromeliad: leaf and root efficiency. Plant Soil 466:293–302
Guo BJ, Li Y, Wang S, Li DF, Lv C, Xu RG (2020) Characterization of the nitrate transporter gene family and functional identification of HvNRT2.1 in barley (Hordeum vulgare L.). PLoS One 15:e0232056
Hassell RL, Memmott F, Liere DG (2008) Grafting methods for watermelon production. Hortic Sci 43:1677–1679
He HY, Xie YY, Zhao AY, Hu WC, Guo X, Miller AJ, Wu XM, Chen BY, Zhang R, Tian H, Gao YJ (2021) Genotypic variation in nitrogen utilization efficiency in oilseed rape is related to the coordination of leaf senescence and root N uptake during reproductive stage. Plant Soil 463:291–306
Hirel B, Tetu T, Lea PJ, Dubois F (2011) Improving nitrogen use efficiency in crops for sustainable agriculture. Sustainability 3:1452–1485
Huang Y, Jiao YY, Nawaz MA, Chen C, Liu L, Lu Z, Kong QS, Cheng F, Bie ZL (2016) Improving magnesium uptake, photosynthesis and antioxidant enzyme activities of watermelon by grafting onto pumpkin rootstock under low magnesium. Plant Soil 409:229–246
Huang Y, Li J, Hua B, Liu ZX, Fan ML, Bie ZL (2013) Grafting onto different rootstocks as a means to improve watermelon tolerance to low potassium stress. Sci Hort 149:80–85
Hussain S, Iqbal N, Brestic M, Raza MA, Pang T, Langham DR, Safdar ME, Ahmed S, Wen BX, Gao Y, Liu WG, Yang WY (2019) Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment. Sci Total Environ 658:626–637
Iqbal A, Dong Q, Alamzeb M, Wang XR, Gui HP, Zhang HH, Pang NC, Zhang XL, Song MZ (2019) Untangling the molecular mechanisms and functions of nitrate to improve nitrogen use efficiency. J Sci Food Agric 100:904–914
Iqbal A, Dong Q, Wang Z, Wang XR, Gui HP, Zhang HH, Pang NC, Zhang XL, Song MZ (2020) Growth and nitrogen metabolism are associated with nitrogen-use efficiency in cotton genotypes. Plant Physiol Biochem 149:61–74
Jacquot A, Chaput V, Mauries A, Li Z, Tillard P, Fizames C, Bonillo P, Bellegarde F, Laugier E, Santoni V, Hem S, Martin A, Gojon A, Schulze W, Lejay L (2020) NRT2.1 C-terminus phosphorylation prevents root high affinity nitrate uptake activity in Arabidopsis thaliana. New Phytol 228:1038–1054
Jiang SY, Sun JY, Tian ZW, Hu H, Michel EJS, Gao JW, Jiang D, Cao WX, Dai TB (2017) Root extension and nitrate transporter up-regulation induced by nitrogen deficiency improves nitrogen status and plant growth at the seedling stage of winter wheat (Triticum aestivum L.). Environ Exp Bot 141:28–40
Kaur G, Asthir B, Bains NS, Farooq M (2015) Nitrogen nutrition, its assimilation and remobilization in diverse wheat genotypes. Int J Agric Biol 17:531–538
Khavari-Nejad RA, Najafi F, Tofighi C (2009) Diverse responses of tomato to N and P deficiency. Int J Agric Biol 2:209–213
Kong QS, Yuan JX, GaoLY ZhaoS, Jiang W, Huang Y, Bie ZL (2014) Identification of suitable reference genes for gene expression normalization in qRT-PCR analysis in watermelon. PLoS One 9:e90612
Krapp A (2015) Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces. Curr Opin Plant Biol 25:115–122
Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. J Exp Bot 53:773–787
Li WB, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass ADM (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143:425–433
Li H, Yu M, Du XQ, Wang ZF, Wu WH, Quintero FJ, Jin X-H, Li HD, Wang Y (2017) NRT1.5/NPF7.3 functions as a proton-coupled H+/K+ antiporter for K+ loading into the xylem in Arabidopsis. Plant Cell 29:2016–2026
Li WM, Yan MK, Hu BY, Priyadarshani SVGN, Hou ZM, Ojolo SP, Xiong JJ, Zhao HM, Qin Y (2018) Characterization and the expression analysis of nitrate transporter (NRT) gene family in pineapple. Trop Plant Biol 11:177–191
Liang JY, Chen XL, Guo PJ, Ren HZ, Xie ZL, Zhang Z, Zhen A (2021) Grafting improves nitrogen-use efficiency by regulating the nitrogen uptake and metabolism under low-nitrate conditions in cucumber. Sci Hortic 289:110454
Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK, Tillard P, Lin HL, Wang YY, Tsai CB, Gojon A, Tsay YF (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528
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
Lo’ay AA, Abo EL-Ezz SF (2021) Performance of ‘Flame seedless’ grapevines grown on different rootstocks in response to soil salinity stress. Sci Hortic 275:109704
Luo LD, Zheng Y, Gao ZA, Chen Q, Kong XX, Yang YP (2020) Grafting improves drought stress memory by increasing the P5CS1 gene expression in Brassica rapa. Plant Soil 452:61–72
Marschner H (1995) Mineral Nutrition of Higher Plants. Academic Press, London
Martínez-Ballesta MC, Muries B, Mota-Cadenas C, Carvajal M (2010) Physiological aspects of rootstock-scion interactions. Sci Hortic 127:112–118
Nawaz MA, Wang LM, Jiao YY, Chen C, Zhao L, Mei MJ, Yu YL, Bie ZL, Huang Y (2017) Pumpkin rootstock improves nitrogen use efficiency of watermelon scion by enhancing nutrient uptake, cytokinin content, and expression of nitrate reductase genes. Plant Growth Regul 82:233–246
Özmen S, Kanber R, Sarı N, Ünlü M (2015) The effects of deficit irrigation on nitrogen consumption, yield, and quality in drip irrigated grafted and ungrafted watermelon. J Integr Agric 14:966–976
Pacheco-Villalobos D, Hardtke CS (2012) Natural genetic variation of root system architecture from Arabidopsis to Brachypodium: towards adaptive value. Phil Trans R Soc B-Biol Sci 367:1552–1558
Pratelli R, Pilot G (2014) Regulation of amino acid metabolic enzymes and transporters in plants. J Exp Bot 65:5535–5556
Qiao YJ, Yin LN, Wang BM, Ke QB, Deng XP, Wang SW (2019) Melatonin promotes plant growth by increasing nitrogen uptake and assimilation under nitrogen deficient condition in winter wheat. Plant Physiol Biochem 139:342–349
Qin F, Liu G, Huang GQ, Dong TF, Liao YM, Xu X (2018) Zinc application alleviates the adverse effects of lead stress more in female Morus alba than in males. Environ Exp Bot 146:68–76
Rahman M, Islam T, Jett L, Kotcon J (2021) Biocontrol agent, biofumigation, and grafting with resistant rootstock suppress soil-borne disease and improve yield of tomato in West Virginia. Crop Prot 145:105630
Rellán-Álvarez R, Lobet G, Dinneny JR (2016) Environmental control of root system biology. Annu Rev Plant Biol 67:619–642
Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A (2006) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol 140:909–921
Renkema H, Koopmans A, Kersbergen L, Kikkert J, Hale B, Berkelaar E (2012) The effect of transpiration on selenium uptake and mobility in durum wheat and spring canola. Plant Soil 354:239–250
Robredo A, Pérez-López U, Miranda-Apodaca J, Lacuesta M, Mena-Petite A, Muñoz-Rueda A (2011) Elevated CO2 reduces the drought effect on nitrogen metabolism in barley plants during drought and subsequent recovery. Environ Exp Bot 71:399–408
Roca LF, Romero J, Bohórquez JM, Alcántara E, Fernández-Escobar R, Trapero A (2018) Nitrogen status affects growth, chlorophyll content and infection by Fusicladium oleagineum in olive. Crop Prot 109:80–85
Ruiz JM, Belakbir A, Lhpez-Cantarero I, Romero L (1997) Leaf-macronutrient content and yield in grafted melon plants. A model to evaluate the influence of rootstock genotype. Sci Hortic 71:227–234
Ruiz JM, Romero L (1999) Nitrogen efficiency and metabolism in grafted melon plants. Sci Hortic 81:113–123
Sallaku G, Sandén H, Babaj I, Kaciu S, Balliu A, Rewald B (2019) Specific nutrient absorption rates of transplanted cucumber seedlings are highly related to RGR and influenced by grafting method, AMF inoculation and salinity. Sci Hortic 243:177–188
Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 5:4983
Savvas D, Öztekin GB, Tepecik M, Ropokis A, Tüzel Y, Ntatsi G, Schwarz D (2017) Impact of grafting and rootstock on nutrient-to-water uptake ratios during the first month after planting of hydroponically grown tomato. J Horticult Sci Biotechnol 92:294–302
Siddiqi MY, Glass ADM (1981) Utilization index: a modified approach to the estimation and comparison of nutrient utilization efficiency in plants. J Plant Nutr 4:289–302
Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581:2290–2300
Tong JF, Walk TC, Han PP, Chen LY, Shen XJ, Li YS, Gu CM, Xie LH, Hu XJ, Liao X, Qin L (2020) Genome-wide identification and analysis of high-affinity nitrate transporter 2 (NRT2) family genes in rapeseed (Brassica napus L.) and their responses to various stresses. BMC Plant Biol 20:464
Van der Vliet L, Peterson C, Hale B (2007) Cd accumulation in roots and shoots of durum wheat: the roles of transpiration rate and apoplastic bypass. J Exp Bot 58:2939–2947
Wang RC, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491–1509
Wang YY, Cheng YH, Chen KE, Tsay YF (2018) Nitrate transport, signaling, and use efficiency. Annu Rev Plant Biol 69:85–122
Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17(8):458–467
Xu GH, Fan XR, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182
Xu X, Li YX, Wang BX, Hu JY, Liao YM (2015) Salt stress induced sex-related spatial heterogeneity of gas exchange rates over the leaf surface in Populus cathayana Rehd. Acta Physiol Plant 37:1709
Yang YJ, Lu XM, Yan B, Li B, Sun J, Guo SR, Tezuka T (2013) Bottle gourd rootstock-grafting affects nitrogen metabolism in NaCl-stressed watermelon leaves and enhances short-term salt tolerance. J Plant Physiol 170:653–661
Yin LP, Li P, Wen B, Taylor D, Berry JO (2007) Characterization and expression of a high-affinity nitrate system transporter gene (TaNRT2.1) from wheat roots, and its evolutionary relationship to other NTR2 genes [J]. Plant Sci 172:621–631
Yuan LY, Zhu SD, Li SH, Shu S, Sun J, Guo SR (2014) 24-Epibrassinolide regulates carbohydrate metabolism and increases polyamine content in cucumber exposed to Ca(NO3)2 stress. Acta Physiol Plant 36:2845–2852
Zhang ZH, Cao BL, Chen ZJ, Xu K (2022) Grafting enhances the photosynthesis and nitrogen absorption of tomato plants under low-nitrogen stress. J Plant Growth Regul 41:1714–1725
Zhang ZH, Li MM, Cao BL, Chen ZJ, Xu K (2021) Grafting improves tomato yield under low nitrogen conditions by enhancing nitrogen metabolism in plants. Protoplasma 258:1077–1089
Zhen A, Bie ZL, Huang Y, Liu ZX, Li Q (2010) Effects of scion and rootstock genotypes on the antioxidant defense systems of grafted cucumber seedlings under NaCl stress. Soil Sci Plant Nutr 56:263–271
Zhen A, Zhang Z, Jin XQ, Liu T, Ren WQ, Hu XH (2018) Exogenous GABA application improves the NO3–N absorption and assimilation in Ca(NO3)2-treated muskmelon seedlings. Sci Hortic 227:117–123
Zou X, Liu MY, Wu WH, Wang Y (2019) Phosphorylation at Ser28 stabilizes the Arabidopsis nitrate transporter NRT2.1 in response to nitrate limitation. J Integr Plant Biol 62:865–876
Acknowledgements
This work was supported by the Basic Research Program of Natural Science in Shaanxi Province (2021JQ-142), the Shaanxi Innovative Research Team (2021TD-34), Shaanxi Agricultural Science and Technology Innovation Project (NYKJ-2021-YL(XN)04), and Xi'an Science and Technology Plan (21NYYF0031).
Funding
This work was supported by the Basic Research Program of Natural Science in Shaanxi Province (2021JQ-142), the Shaanxi Innovative Research Team (2021TD-34), Shaanxi Agricultural Science and Technology Innovation Project (NYKJ-2021-YL(XN)04), and Xi'an Science and Technology Plan (21NYYF0031).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation and data collection were performed by Xiaoling Chen, Peijin Guo, Zhiyu Wang and Wenwen He. Jiayi Liang and Guohu Li analyzed the data. Xiaoling Chen wrote this manuscript. Ai zhen designed the experiment and revised this manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval
This research did not involve human participants or animals.
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Richard J. Simpson.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chen, X., Guo, P., Wang, Z. et al. Grafting improves growth and nitrogen-use efficiency by enhancing NO3− uptake, photosynthesis, and gene expression of nitrate transporters and nitrogen metabolizing enzymes in watermelon under reduced nitrogen application. Plant Soil 480, 305–327 (2022). https://doi.org/10.1007/s11104-022-05583-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05583-2