Skip to main content

Advertisement

SpringerLink
Log in

Grafting improves tomato yield under low nitrogen conditions by enhancing nitrogen metabolism in plants

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

To alleviate the effects of increasingly severe environmental conditions and meet the increasing demand for organic agricultural products, this paper studied tomato grafting under low nitrogen conditions in an effort to enhance yield and improve fruit quality by enhancing nitrogen metabolism. In this study, we screened for two tomato genotypes, a high nitrogen use efficiency genotype (‘TMS-150’) and a low nitrogen use efficiency genotype (‘0301111’), using rootstocks from 25 tomato genotypes and studied the effects of tomato grafting on plant yield, fruit quality, nitrogen content, activities of key nitrogen metabolism enzymes, and nitrogen use efficiency (NUE) under different nitrogen fertilizer conditions. The results showed that the yield of the tomato plants, the activities of key enzymes during nitrogen metabolism, the contents of different forms of nitrogen, and the efficiency of nitrogen use were lower at low nitrogen fertilization levels and higher at higher nitrogen fertilization levels, while the measured indicators were the highest under the N40 nitrogen fertilizer treatment. Grafting tomatoes with high-NUE tomato seedlings as the rootstock resulted in significant increases in the nitrogen content and the activity of key enzymes, enhanced the NUE of tomato plants, increased tomato yield, and improved fruit quality compared to those of the seedlings grafted with low-NUE rootstock. Our results indicate that tomato plants grafted with high-NUE rootstock presented enhanced absorption and utilization of nitrogen and increased plant yield by promoting nitrogen metabolism at different nitrogen levels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Barbosa N, Portilla E, Buendia HF, Raatz B, Beebe S, Rao I (2018) Genotypic differences in symbiotic nitrogen fixation ability and seed yield of climbing bean. Plant Soil 428(1-2):223–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassi D, Menossi M, Mattiello L (2018) Nitrogen supply influences photosynthesis establishment along the sugarcane leaf. Sci Rep 8(1):2327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Benard C, Gautier H, Bourgaud F, Grasselly D, Navez B, Caris-Veyrat C, Weiss M, Genard M (2009) Effects of low nitrogen supply on tomato (Solanum lycopersicum) fruit yield and quality with special emphasis on sugars, acids, ascorbate, carotenoids, and phenolic compounds. J Agric Food Chem 57(10):4112–4123

    Article  CAS  PubMed  Google Scholar 

  • Berge HFMT, Burgers SLGE, Meer HGVD, Schröder JJ, Schoot JRVD, Dijk WV (2007) Residual inorganic soil nitrogen in grass and maize on sandy soil. Environ Pollut 145(1):–0, 30

  • Bloom AJ, Randall L, Taylor AR, Silk WK (2012) Deposition of ammonium and nitrate in the roots of maize seedlings supplied with different nitrogen salts. J Exp Bot 63(5):1997–2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F (2006) Genotypic difference in nitrogen acquisition ability in maize plants is related to the coordination of leaf and root growth. J Plant Nutr 29(2):317–330

    Article  CAS  Google Scholar 

  • Chen A, Lei B, Hu W, Wang H, Zhai L, Mao Y, Fu B, Zhang D (2018) Temporal-spatial variations and influencing factors of nitrogen in the shallow groundwater of the near shore vegetable field of Erhai Lake, China. Environ Sci Pollut Res 25(5):4858–4870

    Article  CAS  Google Scholar 

  • Choudhari SM, Ananthanarayan L (2007) Enzyme aided extraction of lycopene from tomato tissues. Food Chem 102(1):77–81

    Article  CAS  Google Scholar 

  • Cui Z, Zhang F, Mi G, Chen F, Fei L, Chen X, Li J, Shi L (2009) Interaction between genotypic difference and nitrogen management strategy in determining nitrogen use efficiency of summer maize. Plant Soil 317(2):267–276

    Article  CAS  Google Scholar 

  • Deng Z, Cui Y, Han Q, Fang W, Li J, Tian J (2017) Discovery of consistent QTLs of wheat spike-related traits under nitrogen treatment at different development stages. Front Plant Sci 8:2120

    Article  PubMed  PubMed Central  Google Scholar 

  • Duan PF (2019) Response of maize genotypes with different nitrogen use efficiency to low nitrogen stresses. Acta Ecol Sin 39(1):77–80

    Article  Google Scholar 

  • Dwivedi BS, Singh VK, Meena MC, Dey A, Datta SP (2016) Integrated nutrient management for enhancing nitrogen use efficiency. Indian J Fertil 12:62–71

    Google Scholar 

  • Fageria NK, De Morais OP, Dos Santos AB (2010) Nitrogen use efficiency in upland rice genotypes. J Plant Nutr 33(11):1696–1711

    Article  CAS  Google Scholar 

  • Fernández-García N, Martínez V, Cerdá A, Carvajal M (2002) Water and nutrient uptake of grafted tomato plants grown under saline conditions. J Plant Physiol 159(8):899–905

    Article  Google Scholar 

  • Ge S, Ren Y, Peng L, Xu H, Ji M, Wei S, Jiang Y (2014) Effects of Soil C/N Ratio on Apple Growth and Nitrogen Utilization, Residue and Loss. Asian Agric Res 6(1812-2016-143279):69–76

    Google Scholar 

  • Gips CH, Reitsema A, Wibbens-Alberts M (1970) Preservation of urine for ammonia determination with a direct method. Clin Chim Acta 29(3):501–505

    Article  CAS  PubMed  Google Scholar 

  • Gisbert C, Prohens J, Raigón MD, Stommel JR, Nuez F (2011) Eggplant relatives as sources of variation for developing new rootstocks: Effects of grafting on eggplant yield and fruit apparent quality and composition. Sci Hortic 128(1):14–22

    Article  Google Scholar 

  • Hernández V, Hellín P, Fenoll J, Flores P (2019) Interaction of nitrogen and shading on tomato yield and quality. Sci Hortic 255:255–259

    Article  CAS  Google Scholar 

  • Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5(7):304–308

    Article  CAS  PubMed  Google Scholar 

  • Jabnoun-Khiareddine H, Abdallah RAB, Nefzi A, Ayed F, Daami-Remadi M (2019) Grafting tomato cultivars for soilborne disease suppression and plant growth and yield improvement. J Plant Pathol Microbiol 10:1–473

    Google Scholar 

  • Jensen LS, Schjørring JK, van Der Hoek KW, Poulsen HD, Zevenbergen JF, Pallière C, Brentrup F, Jongbloed AW, Willems J, Van Grinsven H (2011) Benefits of nitrogen for food, fibre and industrial production. Cambridge University Press, pp 32–61

  • Karki S, Poudel NS, Bhusal G, Simkhada S, Regmi BR, Adhikari B, Poudel S (2018) Growth parameter and yield attributes of rice (Oryza sativa) as influenced by different combination of nitrogen sources. World 6(2):58–64

    Google Scholar 

  • Kumar P, Edelstein M, Cardarelli M, Ferri E, Colla G (2015) Grafting affects growth, yield, nutrient uptake, and partitioning under cadmium stress in tomato. HortScience 50(11):1654–1661

    Article  CAS  Google Scholar 

  • Kumar P, Rouphael Y, Cardarelli M, Colla G (2017) Vegetable grafting as a tool to improve drought resistance and water use efficiency. Front Plant Sci 8:1130

    Article  PubMed  PubMed Central  Google Scholar 

  • Kunwar S, Paret ML, Freeman JH, Ritchie L, Olson SM, Colee J, Jones JB (2017) Foliar applications of acibenzolar-S-methyl negatively affect the yield of grafted tomatoes in fields infested with Ralstonia solanacearum. Plant Dis 101(6):890–894

    Article  CAS  PubMed  Google Scholar 

  • Kyriacou MC, Soteriou GA, Rouphael Y, Siomos AS, Gerasopoulos D (2016) Configuration of watermelon fruit quality in response to rootstock-mediated harvest maturity and postharvest storage. J Sci Food Agric 96(7):2400–2409

    Article  CAS  PubMed  Google Scholar 

  • Lasagna M, De Luca DA, Franchino E (2016) Nitrate contamination of groundwater in the western Po Plain (Italy): the effects of groundwater and surface water interactions. Environ Earth Sci 75(3):240

    Article  CAS  Google Scholar 

  • Li P, Dong H, Zheng C, Sun M, Liu A, Wang G, Liu S, Zhang S, Chen J, Li Y, Pang C, Zhao X (2017) Optimizing nitrogen application rate and plant density for improving cotton yield and nitrogen use efficiency in the North China Plain. PLoS One 12(10)

  • Liang Y, Zhao X, Jones AM, Gao Y (2018) G proteins sculp root architecture in response to nitrogen in rice and Arabidopsis. Plant Sci 274:129–136

    Article  CAS  PubMed  Google Scholar 

  • Mansour E, Merwad AMA, Yasin MAT, Abdul-Hamid MIE, El-Sobky EEA, Oraby HF (2017) Nitrogen use efficiency in spring wheat: genotypic variation and grain yield response under sandy soil conditions. J Agric Sci 155(9):17

    Article  Google Scholar 

  • Martinelli G, Dadomo A, De Luca DA, Mazzola M, Lasagna M, Pennisi M, Pilla G, Sacchi E, Saccon P (2018) Nitrate sources, accumulation and reduction in groundwater from Northern Italy: insights provided by a nitrate and boron isotopic database. Appl Geochem 91:23–35

    Article  CAS  Google Scholar 

  • Matejovic I (1995) Total nitrogen in plant material determinated by means of dry combustion: A possible alternative to determination by Kjeldahl digestion. Commun Soil Sci Plant Anal 26(13-14):2217–2229

    Article  CAS  Google Scholar 

  • Pellegrini AFA, Ahlström A, Hobbie SE, Reich PB, Nieradzik LP, Staver AC, Scharenbroch BC, Jumpponen A, Anderegg WRL, Randerson JT, Jackson RB (2018) Fire frequency drives decadal changes in soil carbon and nitrogen and ecosystem productivity. Nature 553(7687):194–198

    Article  CAS  PubMed  Google Scholar 

  • Qin S, Zhang Z, Ning T, Ren S, Su L, Li Z (2013) Abscisic acid and aldehyde oxidase activity in maize ear leaf and grain relative to post-flowering photosynthetic capacity and grain-filling rate under different water/nitrogen treatments. Plant Physiol Biochem 70:69–80

    Article  CAS  PubMed  Google Scholar 

  • Razaq M, Zhang P, Shen H, Salahuddin (2017) Influence of nitrogen and phosphorous on the growth and root morphology of acer mono. PLoS One 12(2):e0171321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ren B, Dong S, Zhao B, Liu P, Zhang J (2017) Responses of nitrogen metabolism, uptake and translocation of maize to waterlogging at different growth stages. Front Plant Sci 8:1216

    Article  PubMed  PubMed Central  Google Scholar 

  • 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(3):399–408

    CAS  Google Scholar 

  • Ropokis A, Ntatsi G, Kittas C, Katsoulas N, Savvas D (2019) Effects of Temperature and Grafting on Yield, Nutrient Uptake, and Water Use Efficiency of a Hydroponic Sweet Pepper Crop. Agronomy 9(2):110

    Article  CAS  Google Scholar 

  • Rouphael Y, Kyriacou MC, Colla G (2018) Vegetable grafting: A toolbox for securing yield stability under multiple stress conditions. Front Plant Sci 8:2255

    Article  PubMed  PubMed Central  Google Scholar 

  • Saleque MA, Naher UA, Islam A, Pathan ABMBU, Hossain ATMS, Meisner CA (2004) Inorganic and organic phosphorus fertilizer effects on the phosphorus fractionation in wetland rice soils. Soil Sci Soc Am J 68(5):1635–1644

    Article  CAS  Google Scholar 

  • Schwarz D, Rouphael Y, Colla G, Venema JH (2010) Grafting as a tool to improve tolerance of vegetables to abiotic stresses: Thermal stress, water stress and organic pollutants. Sci Hortic 127(2):162–171

    Article  CAS  Google Scholar 

  • Singh M, Singh VP, Prasad SM (2016) Responses of photosynthesis, nitrogen and proline metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen supplementation. Plant Physiol Biochem 109:72–83

    Article  CAS  PubMed  Google Scholar 

  • Stein LY, Klotz MG (2016) The nitrogen cycle. Curr Biol 26(3):R94–R98

    Article  CAS  PubMed  Google Scholar 

  • Svečnjak Z, Rengel Z (2006) Nitrogen utilization efficiency in canola cultivars at grain harvest. Plant Soil 283(1-2):299–307

    Article  CAS  Google Scholar 

  • Thomsen HC, Eriksson D, Møller IS, Schjoerring JK (2014) Cytosolic glutamine synthetase: a target for improvement of crop nitrogen use efficiency? Trends Plant Sci 19(10):656–663

    Article  CAS  PubMed  Google Scholar 

  • Tirol-Padre A, Ladha JK, Singh U, Laureles E, Punzalan G, Akita S (1996) Grain yield performance of rice genotypes at suboptimal levels of soil N as affected by N uptake and utilization efficiency. Field Crop Res 46(1-3):127–143

    Article  Google Scholar 

  • Wang Q, Nian J, Xie X, Yu H, Zhang J, Bai J, Dong G, Hu J, Bai B, Chen L, Xie Q, Feng J, Yang X, Peng J, Chen F, Qian Q, Li J, Zuo J (2018) Genetic variations inare1mediate grain yield by modulating nitrogen utilization in rice. Nat Commun 9(1):735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang W, Hao Q, Wang W, Li Q, Chen F, Ni F, Wang FD, Wu JY, Wang W (2019) The involvement of cytokinin and nitrogen metabolism in delayed flag leaf senescence in a wheat stay-green mutant, tasg1. Plant Sci 278:70–79

    Article  CAS  PubMed  Google Scholar 

  • Wei S, Wang X, Shi D, Li Y, Zhang J, Liu P, Zhao B, Dong S (2016) The mechanisms of low nitrogen induced weakened photosynthesis in summer maize (Zea mays L.) under field conditions. Plant Physiol Biochem 105:118–128

    Article  CAS  PubMed  Google Scholar 

  • Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annu Rev Plant Biol 63:153–182

    Article  CAS  PubMed  Google Scholar 

  • Yamaya T, Kusano M (2014) Evidence supporting distinct functions of three cytosolic glutamine synthetases and two nadh-glutamate synthases in rice. J Exp Bot 65(19):5519–5525

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Lu Y, Ding Y, Yin X, Raza S, Tong Y’a (2017) Optimising nitrogen fertilisation: a key to improving nitrogen-use efficiency and minimising nitrate leaching losses in an intensive wheat/maize rotation (2008–2014). Field Crop Res 206:1–10

    Article  Google Scholar 

  • Yin F, Liu X, Cao B, Xu K (2019) Low pH altered salt stress in antioxidant metabolism and nitrogen assimilation in ginger (Zingiber officinale) seedlings. Physiol Plant. https://doi.org/10.1111/ppl.13011

  • Zhang H, Fu X, Wang X, Gui H, Dong Q, Pang N, Wang Z, Zhang X, Song M (2018) Identification and screening of nitrogen-efficient cotton genotypes under low and normal nitrogen environments at the seedling stage. J Cotton Res 1(1)

  • Zhang Z, Cao B, Gao S, Xu K (2019) Grafting improves tomato drought tolerance through enhancing photosynthetic capacity and reducing ROS accumulation. Protoplasma 256(4):1013–1024

    Article  CAS  PubMed  Google Scholar 

  • Zhao SJ, Shi GA, Dong XC (2002) Techniques of Plant Physiological Experiment. Beijing: Chinese Agricultural Science and Technology Press. (in Chinese)

Download references

Funding

This work was supported by the Double First-class Discipline Construction Project of Shandong Province (No. SYL2017YSTD06).

Author information

Authors and Affiliations

  1. College of Horticulture Science and Engineering, Shandong Agricultural University, 271018, Tai’an, People’s Republic of China

    Zhi Huan Zhang, Bi Li Cao, Zi Jing Chen & Kun Xu

  2. Collaborative Innovation Center of Fruit and Vegetable Quality and Efficient Production, Tai’an, Shandong, People’s Republic of China

    Zhi Huan Zhang, Bi Li Cao, Zi Jing Chen & Kun Xu

  3. State Key Laboratory of Crop Biology, Key Laboratory of Biology and Genetic Improvement of Horticultural Crops in Huanghuai Region, Ministry of Agriculture and Rural Affairs, Beijing, People’s Republic of China

    Zhi Huan Zhang, Bi Li Cao, Zi Jing Chen & Kun Xu

  4. Taishan Property Insurance Co., Ltd., Jinan, People’s Republic of China

    Ming Ming Li

Authors
  1. Zhi Huan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ming Ming Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bi Li Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zi Jing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Kun Xu designed experiments; Zhi Huan Zhang, Ming Ming Li, Bili Cao, and Zi Jing Chen complete the experiments; Zhi Huan Zhang and Kun Xu wrote the manuscript.

Corresponding author

Correspondence to Kun Xu.

Additional information

Handling Editor: Hanns H. Kassemeyer

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Z.H., Li, M.M., Cao, B.L. et al. Grafting improves tomato yield under low nitrogen conditions by enhancing nitrogen metabolism in plants. Protoplasma 258, 1077–1089 (2021). https://doi.org/10.1007/s00709-021-01623-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-021-01623-3

Keywords

Search

Navigation