The Potential of Nitrate Accumulation in Plants and the Effects of Nitrate on Human Health

Abstract

Plants take nitrogen (N) from the soil through their roots throughout their life cycle. The amount and uptake form of nitrogen, an essential nutrient, significantly influence plant growth and their interactions with the environment. In soil, N is present in inorganic forms such as nitrate (NO3−) and ammonium (NH4+), but can also be found in organic forms such as urea, free amino acids and short peptides. Nitrate (NO3−) is a very important form of nitrogen for all plants due to its role in plant nutrition and physiology. Leafy vegetables have a very important place in the human diet, but they are a food group that contributes greatly to nitrate (NO3−) uptake by living organisms. Exogenous nitrate concentrations are among the most important factors influencing NO3− accumulation in plants. Leafy vegetables can accumulate high amounts of nitrates if nitrogen fertilisation is excessive. Nitrate-containing foods consumed by humans can pose serious health risks. This review focuses on nitrate assimilation and transport in plants, nutritional, environmental and physiological factors affecting nitrate accumulation, the contribution of vegetables to nitrate uptake in humans, and the harmful and beneficial effects of nitrate on human health.

Keywords

• Nitrate assimilation and transport
• Nitrate toxicity
• Nİtrate reductase
• Leafy vegetables
• Human health

Bitkilerde Nitrat Birikim Potansiyeli ve Nitratın İnsan Sağlığı Üzerindeki Etkileri

Öz

Bitkiler tüm yaşam döngüleri boyunca kökleri aracılığıyla topraktan azot (N) alırlar. Temel bir besin elementi olan azotun miktarı ve alınma formu, bitki büyümesini ve onun çevresiyle olan etkileşimlerini önemli ölçüde etkiler. Toprakta N; nitrat (NO3−) ve amonyum (NH4+) gibi inorganik formlarda bulunmakla birlikte üre, serbest amino asitler ve kısa peptidlerden oluşan organik formlarda da bulunabilmektedir. Nitrat (NO3−), bitki beslenmesindeki ve fizyolojisindeki rolü nedeniyle tüm bitkiler için çok önemli bir azot formudur. Yapraklı sebzeler insanların beslenmesinde çok önemli bir yer tutmakla birlikte canlıların nitrat (NO3−) alımına yüksek seviyelerde katkı sağlayan bir besin grubunu da oluşturmaktadır. Nitratın eksojen konsantrasyonları, bitkilerde NO3− birikimini etkileyen en önemli faktörler arasındadır. Azotlu gübrenin aşırı uygulanması durumunda yapraklı sebzeler yüksek düzeyde nitrat biriktirebilir. İnsanlar tarafından tüketilen nitrat bakımından zengin besinler ciddi sağlık tehlikeleri oluşturabilir. Bu derleme çalışması, bitkilerde nitrat asimilasyonu ve taşınımı, nitrat birikimini etkileyen besinsel, çevresel ve fizyolojik faktörler, insanların diyetle nitrat alımına sebzelerin katkısı ve nitratın insan sağlığı üzerindeki zararlı ve faydalı etkileri üzerine odaklanmaktadır.

Anahtar Kelimeler

• Nitrat asimilasyonu ve taşınımı
• nitrat toksisitesi
• nitrat redüktaz
• yapraklı sebzeler
• insan sağlığı

Kaynakça

1. Ahmed AHH. Physiological studies on tipburn and nitrate accumulation in lettuce plants. Mansoura University Journal of Agricultural Sciences 1996; 21: 3971-3994.
2. Ahmed AHH., Khalil MK., Farrag AM. Nitrate accumulation, growth, yield and chemical composition of Rocket (Eruca vesicaria subsp. sativa) plant as affected by NPK fertilization, kinetin and salicylic acid. In: Proceedings of ICEHM 2000, page no: 495-508, Cairo University, Egypt.
3. Ali A. Nitrate assimilation pathway in higher plants: critical role in nitrogen signalling and utilization. Plant Science Today 2020; 7(2): 182-192.
4. Ali A., Sivakami S., Raghuram N. Effect of nitrate, nitrite, ammonium, glutamate, glutamine and 2-oxoglutarate on the RNA levels and enzyme activities of nitrate reductase and nitrite reductase in rice. Physiology and Molecular Biology of Plants 2007; 13(1): 17-25.
5. Andrews M. The partitioning of nitrate assimilation between root and shoot of higher plants: mini review. Plant Cell and Environment 1986; 9: 511-519.
6. Anjana SU, Iqbal M. Nitrate accumulation in plants, factors affecting the process, and human health implications. A review. Agronomy for Sustainable Development 2007; 27: 45-57.
7. Anjana Umar S., Iqbal M., Abrol YP. Are nitrate concentrations in leafy vegetables within safe limits? Proceedings of the workshop on nitrogen in environment, industry and agriculture, 2006, page no: 81-84, New Delhi, India.
8. ATSDR (Agency for Toxic Substances and Diseases Registry). Case studies in environmental medicine: Nitrate/nitrite toxicity. US Department of Health and Human Services, Atlanta; 2001.

9. Badawi AF., Gehen H., Mohamed EH., Mostafa HM. Salivary nitrate, nitrite and nitrate reductase activity in relation to risk of oral cancer in Egypt. Disease Markers 1998; 14: 91-97.
10. Battye W., Aneja PV., Schlesinger WH. Is nitrogenthe next carbon? Earth’s Future 2017; 5: 894-904,
11. Behr U., Wiebe HJ. Relation between photosynthesis and nitrate content of lettuce cultivars. Scientia Horticulturae 1992; 49: 175-179.
12. Bian Z., Wang Y., Zhang X., Li T., Grundy S., Yang Q., Cheng R. A review of environment effects on nitrate accumulation in leafy vegetables grown in controlled environments. Foods 2020; 9(6), 732.
13. Bjorne H., Petersson J., Phillipson M., Weitzberg E., Holm L., Lundberg JO. Nitrate in saliva increases gastric mucosal blood flow and mucus thickness. The Journal of Clinical Investigation 2004; 113: 106-114.
14. Blom-Zandstra M. Nitrate accumulation in vegetables and its relationship to quality. Annals of Applied Biology 1989; 115: 553-561.
15. Blom-Zandstra M., Eenink AH. Nitrate concentration and reduction in different genotypes of lettuce. Journal of the American Society for Horticultural Science 1986; 111: 908-911.
16. Blom-Zandstra M., Lampe JEM. The effect of chloride and sulphate salts on the nitrate content in lettuce plants. Journal of Plant Nutrition 1983; 6: 611-628.
17. Bondonno CP., Croft KD., Hodgson JM. Dietary nitrate, nitric oxide, and cardiovascular health. Critical Reviews in Food Science and Nutrition 2016; 56(12): 2036-2052.
18. Bowsher CG., Lacey AE., Hanke GT., Clarkson DT. Saker LR., Stulen I., Emes MJ. The effect of Glc6P uptake and its subsequent oxidation within pea root plastids on nitrite reduction and glutamate synthesis. Journal of Experimental Botany 2007; 58(5): 1109-1118.
19. Buwalda F., Warmenhoven M. Growth-limiting phosphate nutrition suppresses nitrate accumulation in greenhouse lettuce. Journal of Experimental Botany 1999; 50: 813-821.
20. Cantliffe DJ. Nitrate accumulation in table beets and spinach as affected by nitrogen, phosphorus, and potassium nutrition and light intensity. Agronomy Journal 1973; 65: 563-565.
21. Cardenas-Navarro R., Adamowicz S., Robin P. Nitrate accumulation in plants: a role for water. Journal of Experimental Botany 1999; 50: 613-624.
22. Cerezo M., Garcia-Agustin P., Serna MD., Primo-Millo E. Kinetics of nitrate uptake by citrus seedlings and inhibitory effects of salinity. Plant Science 1997; 126: 105-112.
23. Chadjaa H., Vezina LP., Dorais M., Gosselin A. Effects of lighting on the growth, quality and primary nitrogen assimilation of greenhouse lettuce (Lactuca sativa L.). Acta Horticulturae 2001; 559: 325-331.
24. Chapagain BP., Wiesman Z., Zaccai M., Imas P., Magen H. Potassium chloride enhances fruit appearance and improves quality of fertigated greenhouse tomato as compared to potassium nitrate. Journal of Plant Nutrition 2003; 26: 643-658.
25. Chen BM., Wang ZH., Li SX., Wang GX., Song HX., Wang XN. Effects of nitrate supply on plant growth, nitrate accumulation, metabolic nitrate concentration and nitrate reductase activity in three leafy vegetables. Plant Science 2004; 167: 635-643.
26. Chen KE., Chen HY., Tseng CS., Tsay YF. Improving nitrogen use efficiency by manipulating nitrate remobilization in plants. Nature Plants 2020; 6(9): 1126-1135.
27. Chung JB., Jin SJ., Cho HJ. Low water potential in saline soils enhances nitrate accumulation of lettuce. Communications in Soil Science and Plant Analysis 2005; 36: 1773-1785.
28. Chung SY., Kim JS., Kim M., Hong MK., Lee JO., Kim CM., Song IS. Survey of nitrate and nitrite contents of vegetables grown in Korea. Food Additives & Contaminants 2003; 20: 621-628.
29. Colla G., Cardona Suárez CM., Cardarelli M., Rouphael Y. Improving nitrogen use efficiency in melon by grafting. HortScience 2010; 45: 559-565.
30. Colla G., Kim HJ., Kyriacou MC., Rouphael Y. Nitrate in fruits and vegetables. Science Horticulturae (Amsterdam) 2018; 237: 221-238.
31. Conde A., Diallinas G., Chaumont F., Chaves M. Gerós H. Transporters, channels, or simple diffusion? Dogmas, atypical roles and complexity in transport systems. The International Journal of Biochemistry & Cell Biology 2010; 42(6): 857-868.
32. Croen LA., Todoroff K., Shaw GM. Maternal exposure to nitrate from drinking water and diet and risk for neural tube defects. American Journal of Epidemiology 2001; 153: 325-331.
33. Cui J., Yu C., Qiao N., Xu X., Tian Y., Ouyang H. Plant preference for NH4+ versus NO3− at different growth stages in an alpine agroecosystem. Field Crops Research 2017; 201: 192-199,
34. Curran A., Chang IF., Chang CL., Garg S., Miguel RM., Barron YD., Li Y., Romanowsky S., Cushman JC., Gribskov M., Harmon AC., Harper JF. Calcium-dependent protein kinases from Arabidopsis show substrate specificity differences in an analysis of 103 substrates. Frontiers in Plant Science 2011; 2, 36.
35. Custic M., Poljak M., Coga L., Cosic T., Toth N., Pecina M. The influence of organic and mineral fertilization on nutrient status, nitrate accumulation, and yield of head chicory. Plant Soil and Environment 2003; 49: 218-222.
36. Dodd IC., Tan LP., He J. Do increases in xylem sap pH and/or ABA concentration mediate stomatal closure following nitrate deprivation?. Journal of Experimental Botany 2003; 54(385): 1281-1288.
37. Dorais M., Papadoulos AP., Gosselin A. Greenhouse tomato fruit quality. Horticultural Reviews 2001; 26: 262-319.
38. Drlik J., Rogl J. The effect of graduated rates of nitrogen fertilization on yield and nitrate accumulation in carrots. Zahradnictvi 1992; 19: 39-46.
39. Duncan C., Dougall H., Johnston P., Green S., Brogan R., Leifert C., Smith L., Golden M., Benjamin N. Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nature Medicine 1995; 1: 546-551.
40. Duncan C., Li H., Dykhuizen R., Frazer R., Johnston P., MacKnight G., Smith L., Lamza K., McKenzie H., Batt L., Kelly D., Golden M., Benjamin N., Leifert C. Protection against oral and gastrointestinal diseases: importance of dietary nitrate intake, oral nitrate reduction and enterosalivary nitrate circulation. Comparative Biochemistry and Physiology 1997; 118: 939-948.
41. Dykhuizen R., Frazer R., Duncan C., Smith CC., Golden M., Benjamin N., Leifert C. Antimicrobial effect of acidified nitrite on gut pathogens: importance of dietary nitrate in host defence. Antimicrobial Agents and Chemotherapy 1996; 40: 1422-1425.
42. EFSA. Opinion of the scientific panel on contaminants in the food chain on a request from the European Commission to perform a scientific risk assessment on nitrate in vegetables. EFSA J 2008; 689: 1-79.
43. Eicholzer M., Gutzwiller F. Dietary nitrates, nitrites and N-nitroso compounds and cancer risk: A review of the epidemiologic evidence. Nutrition Reviews 1990; 56: 95-105.
44. Elia A., Conversa G., Gonnella M. Dosi di azoto, produzione e accumulo di nitrati di lattuga allevata in idrocoltura, Atti V Giornate Scientifiche SOI, Sirmione 2000; 229-230.