Bitkilerde Bor Toksisitesi ve Bor Toleransı

Öz

Bor periyodik tablonun 3A grubunda bulunan ve metaloid olarak kabul edilen bir elementtir. Bor doğada oksijenle birleşmiş olarak boratlar ve daha seyrek olarak boric asit veya florinle bileşik oluşturmuş halde bulunur. Bor bitkilerde normal büyüme ve gelişme için gereksinim duyulan bir mikroelementtir. Borun bitkilerde karbohidrat metabolizması, hücre çeperi sentezi, plazma membranının bütünlüğünün ve fonksiyonunun sürekliliği, nükleik asit, azot, fenolik madde ve oksin metabolizması, polen tüpü oluşumu, askorbat-glutatyon döngüsü ve fotosentez gibi konularda önemli fonksiyonları vardır. Ancak toprakta aşırı miktarda borun bulunması hücresel metabolizmada bozukluklara neden olabilir. Bor toksisitesinin bitkilerdeki primer fenotipik etkisi kök büyümesinin inhibisyonu ve kök kuru ağırlığının azalmasıdır. Ayrıca bor toksisitesi tarımsal öneme sahip olan bitkilerde oksidatif strese neden olur ve fotosentetik aktiviteyi azaltabilir. Bitkilerdeki bor tolerans mekanizması oldukça karmaşıktır ve henüz tam olarak anlaşılamamıştır. Borun toprakdan suyla süzülerek uzaklaştırılması ve boru inaktif veya hareketsiz hale getirmek için yapılan uygulamalar uzun süre bor toksisitesini engellemek amacıyla kullanılmıştır. Ancak bu konudaki en gerçekçi yaklaşım tarımsal üretimi artırmak amacıyla bora toleranslı bitki genotiplerinin seleksiyonudur. Bu çalışmada bor elementinin bitkilerdeki fizyolojik fonksiyonları, bor toksisitesi semptomları ve tolerans mekanizmaları tartışılmıştır.

Anahtar Kelimeler

• Bor
• Hücre çeperi
• Plazma zarı
• Bor toleransı
• Bor toksisitesi

Boron Toxicity and Boron Tolerance in Plants

Öz

Boron is an element that is considered as a metalloid and belongs to third A group in the periodic table. It occurs in nature in combination with oxygen as borates and less frequently boric acid or associated with fluorine. Boron is a micronutrient for plants necessary for normal growth and development. It has very important functions including carbohydrate metabolism, cell wall synthesis, the maintanence of plasma membrane integrity and functions, nucleic acid, nitrogen, phenolic and auxine metabolism, polen tube formation, ascorbate-glutathione cycle and photosynthesis. However, cellular metabolism could be impaired as a result of excess boron in soil. The primary phenotypic effect of boron toxicity is the inhibition of root growth and decreased dry weight of roots. In addition, boron toxicity could cause oxidative stress and lower photosynthetic activity in crop plants. The mechanism of boron tolerance in plants is very complex and has not been yet understood in details. Soil amendment such as leaching boron with water and application of some organic compounds to inactivate or immobilize boron in soils has been used to solve boron toxicity in plants for many years. However, it appears that the most realistic way to improve crop yield is the selection of boron tolerant genotypes. In this review, the physiological functions of boron in plants, toxicity symptoms and tolerance mechanisms has been discussed.

Anahtar Kelimeler

• Boron
• Cell wall
• Plasma membrane
• Boron tolerance
• Boron toxicity

Kaynakça

1. Aftab T., Khan MMA., Idrees M., Naeem M., Moinuddin NH. Methyl jasmonate counteracts boron toxicity by preventing oxidative stress and regulating antioxidant enzyme activities and artemisinin biosynthesis in Artemisia annua L. Protoplasma 2011; 248(3): 601-612.
2. Aftab T., Khan MMA., Naeem M., Idrees M., da Silva JAT., Ram M. Exogenous nitric oxide donor protects Artemisia annua from oxidative stress generated by boron and aluminium toxicity. Ecotoxicology and Environmental Safety 2012; 80: 60-68.
3. Aftab T., Landi M., Papadakis IE., Araniti F., Brown PH. Boron in plants and agriculture. Academic Press: London; 2022.
4. Andreon Viçosi K., dos Santos de Carvalho A., Castilho Silva D., de Paula Almeida F., Ribeiro D., Alves Flores R. Foliar fertilization with boron on the growth, physiology, and yield of snap beans. Journal of Soil Science and Plant Nutrition 2020; 20(3): 917-924.
5. Aquea F., Federici F., Moscoso C., Vega A., Jullian P., Haseloff J., Arce-Johnson P. A molecular framework for the inhibition of Arabidopsis root growth in response to boron toxicity. Plant Cell an Environment 2012; 35: 719-734.
6. Archana NP., Verma P. Boron deficiency and toxicity and their tolerance in plants: A review. Journal of Global Bioscience 2017; 6: 4958-4965.
7. Arredondo G., Bonomelli C. Effect of three boron conconcentrations in soil on growth and physiology in sweet cherry trees. Plants 2023; 12(6): 1240.
8. Arunkumar B., Thippeshappa G., Anjali M., Prashanth K. Boron: A critical micronutrient for crop growth and productivity. Journal of Pharmacognosy Phytochemistry 2018; 7: 2738-2741.

9. Begum RA., Fry SC. Arabinogalactan-proteins as boron-acting enzymes, cross-linking the rhamnogalacturonan-II domains of pectin. Plants 2023; 12(23): 3921.
10. Bildiren Ş. Tuz stresi altındaki farklı buğday (Triticum aestivum L.) genotiplerinde bor uygulamalarının iyileştirici etkisinin araştırılması. Sakarya Üniversitesi Fen Bilimleri Enstitüsü Yüksek Lisans Tezi, sayfa no:137, Sakarya, Türkiye, 2018.
11. Bita A., Scorei IR., Ciocilteu MV., Nicolescu OE., Pirvu AS., Bejenaru LE., Rau G., Bejenaru C., Radu A., Neamtu J., Mogoşanu GD., Benner SA. Nicotinamide riboside, a promising vitamin B3 derivative for healthy aging and longevity: Current research and perspectives. Molecules 2023; 28(16): 6078.
12. Bogacki P., Peck DM., Nair RM., Klaus JH., Oldach H. Genetic analysis of tolerance to boron toxicity in the legume Medicago truncatula. BMC Plant Biology 2013; 13: 54.
13. Bolan S., Wijesekara H., Amarasiri D., Zhang T., Regalyi P., Brdar-Jokanovic M., Rekasi M., Lin JY., Padhye LP., Zhao H., Wang L., Rinklebe J., Wang H., Siddique KHM., Kirkham MB., Bolan N. Boron contamination and its risk management in terrestrial and aquatic environmental settings. Sceince of the Total Environment 2023; 894: 164744.
14. Bolanos L., Abreu I., Bonilla I., Cristobal JJC., Reguero M. What can boron deficiency symptoms tell us about its function and regulation? Plants 2023; 12(4): 777.
15. Bolanos L., Lukaszewski K., Bonilla I., Blevins D. Why boron? Plant Physiology and Biochemistry 2004; 42: 907-912.
16. Bonilla I., Blevins D., Bolanos L. Boron functions in plants: looking beyond the cell wall. In: Taiz, L., Zeiger, E. (Eds.), Plant Physiology, 4th ed: IOP Publishing; 2009.
17. Camacho-Cristóbal JJ., Navarro-Gochicoa MT., Rexach J., González Fontes A., Herrera-Rodríguez MB. Plant response to boron deficiency and boron use efficiency in crop plants. Plant micronutrient use efficiency. Elsevier 2018; 109-121.
18. Cervilla LM., Blasco B., Rios JJ., Rubio-Wilhelmi MM., Sanchez-Rodriguez E., Romero L., Ruiz JM. Response of nitrogen metabolism to boron toxicity in tomato plants. Plant Biology 2009; 11: 671-677.
19. Cervilla LM., Rosales MA., Rubio-Wilhelmi MM., Sanchez-Rodriguez E., Blasco B., Rios JJ., Romero L., Ruiz JM. Involvement of lignification and membrane permeability in the tomato root response to boron toxicity. Plant Science: An International Journal of Experimental Plant Biology 2009; 176(4): 545-552.
20. Chatzistathis T., Fanourakis D., Aliniaeifard S., Kotsiras A., Delis C., Tsaniklidis G. Leaf age-dependent effects of boron toxicity in two Cucumis melo varieties. Agronomy 2021; 11(4): 759.
21. Chen M., Mishra S., Heckathorn SA., Frantz JM., Krause C. Proteomic analysis of Arabidopsis thaliana leaves in response to acute boron deficiency and toxicity reveals effects on photosynthesis, carbohydrate metabolism, and protein synthesis. Journal of Plant Physiology 2013; 171(3–4): 235-242.
22. Chen X., Schauder S., Potier N., Van Dorsselaer A., Pelczer I., Bassler BL., Hughson FM. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 2002; 415: 545-549.
23. Chen X., Smith SM., Shabala S., Yu M. Phytohormones in plant responses to boron deficiency and toxicity. Journal of Experimental Botany 2022; 74(3): 743-754.
24. Choi EY., Kolesik P., Mcneill A., Collins H., Zhang Q., Huynh BL., Graham R., Stangoulis J. The mechanism of boron tolerance for maintenance of root growth in barley (Hordeum vulgare L.). Plant Cell and Environment 2007; 30: 984-993.
25. Corwin D. Climate change impacts on soil salinity in agricultural areas. European Journal of Soil Science 2021; 72(2): 842-862.
26. Çatav ŞS., Çetin E., Vural E., Bürün B. Boron toxicity tolerance in barley may be related to intrinsically higher levels of reactive oxygen species in the shoots. Botanica Serbica 2023; 47(1): 113-124.
27. Çatav ŞS., Köşkeroğlu S., Tuna AL. Selenium supplementation mitigates boron toxicity induced growth inhibition and oxidative damage in pepper plants. South African Journal of Botany 2022; 146: 375-382.
28. Dannel F., Pfeffer H., Romheld V. Update on boron in higher plant-uptake, primary translocation and compartmentation. Plant Biology 2002; 4: 193-204.
29. De Souza LT., Carr NF., Lavres J., Mazzafera P., Favarin JL. Boron deficiency affects ATP hydrolysis of plasma membrane and nutrients uptake in coffee: Consequences for plant growth. Journal of Plant Nutrition 2022; 45(14): 2123-2134.
30. Emebiri L., Michael P., Moody D. Enhanced tolerance to boron toxicity in two-rowed barley by marker assisted introgression of favorable alleles derived from Sahara 3771. Plant and Soil 2009; 314: 77–85.
31. Estevez L., Queizan M., Mosquera RA., Guidi L., Lo Piccolo E., Landi M. First characterization of the formation of anthocyanin–Ge and anthocyanin–B complexes through UV–vis spectroscopy and density functional theory quantum chemical calculations. Journal of Agriculture and Food Chemistry 2021; 69: 1272-1282.
32. Flores R., Silva Junior AR., Damin V., Arruda EM., Prado ER., Araujo CE. Nutrition and production of Phaseolus vulgaris (BRS Estilo) following boron application on soil. Communications in Soil Science and Plant Analysis 2017; 48(12): 1409-1416.
33. Funakawa H., Miwa K. Synthesis of borate cross-linked rhamnogalacturonan II. Frontiers in Plant Science 2015; 6: 223.
34. Garcia- Sanchez F., Simon-Grao S., Martinez-Nicolas JJ., Alfosea-Simon M., Liu C., Chatzissavvidis C., Camara-Zapata JM. Multiple stresses occuring with boron toxicity and deficiency in plants. Journal of Hazardous Materials 2020; 397: 122713.
35. Goldbach HE., Wimmer M. Boron in plants and animals: Is there a role beyond cell-wall structure? Journal of Plant Nutrition and Soil Science 2007; 170: 39-48.
36. Goldbach HE. Advances in understanding boron cycling in soils, uptake/use by plants and ways of optimizing boron use efficiency in crop production. In: Rengel Z. (ed.) Achieving Sustainable Crop Nutrition. London: Burleigh Dodds Science Publishing 2020; 355-406.
37. Gonzalez-Fontes A., Rexach J., Navarro-Gochicoa MT., Herrera-Rodriguez MB., Beato VM., Maldonado JM., Camacho-Cristobal JJ. Is boron involved solely in structural roles in vascular plants? Plant Signaling and Behavior 2008; 3: 24-26.
38. Grew ES., Bada JL., Hazen RM. Borate minerals and origin of the RNA World. Origins of Life and Evolution of Biosphere 2011; 41: 307-316.
39. Güneş A., Söylemezoğlu G., İnal A., Bağcı EG., Çoban S., Şahin O. Antioxidant and stomatal responses of grapevine (Vitis vinifera L.) to boron toxicity. Scientia Horticulturae 2006; 110: 279-284.
40. Güneş A., Gezgin S., Kalınbacak K., Özcan H., Çakmak İ. Bor elementinin bitkiler için önemi. Bor Dergisi 2017; 2(3): 168-174.
41. Hayes JE., Reid RJ. Boron tolerance in barley is mediated by efflux of boron from the roots. Plant Physiology 2004; 136: 3376-3382s.
42. Hegazi E., El-Motaium R., Yehia T., Hashim M. Effect of foliar boron application on boron, chlorophyll, phenol, sugars and hormones concentration of olive (Olea europaea L.) buds, leaves, and fruits. Journal of Plant Nutrition 2018; 41: 749-765.
43. Helvacı C. Borates. In: Alderton D., Elias SA. (eds.) Encyclopedia of Geology. United Kingdom: Academic Press 2021; 489-504.
44. Hilal N., Kim GJ., Somerfield C. Boron removal from saline water: a comprehensive review. Desalination 2011; 273: 23-35.
45. Hosmane NS. Boron science. New Technologies and Applications. Boca Raton: CRC Press 2012. Hossain MF., Shenggang P., Meiyang D., Zhaowen M., Karbo MB., Bano A., Xiangru T. Photosynthesis and antioxidant response to winter rapeseed (Brassica napus L.) as affected by boron. Pakistan Journal of Botany 2015; 47(2): 675-684.
46. Hua T., Zhang R., Sun H., Liu C. Alleviation of boron toxicityin plants: Mechanisms and approaches. Critical Reviews in Environmental Science and Technology 2021; 51(24): 2975-3015.
47. Huo J., Song B., Riaz M., Song X., Li J., Liu H., Huang W., Jia Q., Wu W. High boron stress leads to sugar beet (Beta vulgaris L.) toxicity by disrupting photosystem Ⅱ. Ecotoxicology and Environmental Safety 2022; 248: 114295. Jothi M., Takano J. Understanding the regulatory mechanisms of B transport to develop crop plants with B efciency and excess B tolerance. Plant and Soil 2023; 487: 1-20.
48. Kajikawa M., Fujibe T., Uraguchi S., Miwa K., Fujiwara T. Expression of the Arabidopsis borate efflux transporter gene, AtBOR4, in rice affects the xylem loading of boron and tolerance to excess boron. Bioscience Biotechnology, and Biochemistry 2011; 75(12): 2421-2423.
49. Karabal E., Yucel M., Oktem HA. Antioxidant responses of tolerant and sensitive barley cultivars to boron toxicity. Plant Science 2003; 164: 925-933.
50. Keleş Y., Öncel I., Yenice N. Relationship between boron content and antioxidant compounds in Citrus leaves taken from fields with different water source. Plant and Soil 2004; 265: 345-353.
51. Kobayashi M., Mutoh T., Matoh T. Boron nutrition of cultured tobacco BY-2 cells. IV Genes induced under low boron supply. Journal of Experimental Botany 2004; 55: 1441-1443.
52. Kohli SK., Kaur H., Khanna K., Handa N., Bhardwaj R., Rinklebe J., Ahmad P. Boron in plants: uptake, deficiency and biological potential. Plant Growth Regulation 2023; 100: 267-282.
53. Kohnehsharhi SM., Demir Y. Glutathione and proline attenuates injury induced by boron toxicity in wheat. Journal of Agricultural Science 2023; 29(2): 371-379.
54. Kumar K., Mosa K., Chhikara S., Musante C., White J., Dhankher O. Two rice plasma membrane intrinsic proteins, OsPIP2;4 and OsPIP2;7, are involved in transport and providing tolerance to boron toxicity. Planta 2014; 239: 187-198.
55. Kumar V., Pandita S., Kaur R., Kumar A., Bhardwaj R. Biogeochemical cycling, tolerance mechanism and phytoremediation strategies of boron in plants: A critical review. Chemosphere 2022; 300: 134505.
56. Landi M., Pardossi A., Remorini D., Guidi L. Antioxidant and photosynthetic response of a purple-leaved and a green-leaved cultivar of sweet basil (Ocimum basilicum) to boron excess. Environmental and Experimental Botany 2013; 85: 64-75.
57. Landi M., Guidi L., Pardossi A., Tattini M., Gould KS. Photoprotection by foliar anthocyanins mitigates effects of boron toxicity in sweet basil (Osimum basilicum). Planta 2014; 240(5): 941-953.
58. Liu C., Lu W., Ma Q., Ma C. Effectf of silicon on the alleviation of boron toxicity in wheat growth, boron accumulation, photosynthesis activities, and antioxidative responses. Journal of Plant Nutrition 2017; 40(17): 2458-2467.
59. Liu J., Chen T., Wang CL., Liu X. Transcriptome analysis in Pyrus betulaefolia roots in response to short-term boron deficiency. Genes 2023; 14: 817.
60. Liu L., Luo Y., Ding G., Wang C., Cai H., Shi L., Xu F., Bao X., Wang S. Identifcation and function characterization of BnaBOR4 genes reveal their potential for Brassica napus cultivation under high boron stress. Ecotoxicology and Environmental Safety 2024; 271: 1160112012.
61. Long Y., Peng J. Interaction between boron and other elements in plants. Genes 2023; 14(1): 130.
62. Matoh T., Kawaguchi S., Kobayashi M. Ubiquity of a boraterhamno-galacturonan II complex in the cell walls of higher plants. Plant and Cell Physiology 1996; 37: 636-640.
63. Matthes M., Torres-Ruiz RA. Boronic acid treatment phenocopies monopteros by affectin PIN1 membrane stability and polar auxin transport in Arabidopsis thaliana embryos. Development 2016; 143: 4053-4062.
64. Mishra S., Heckathorn S., Krause C. The levels of boron-uptake proteins in roots are correlated with tolerance to boron stress in barley. Crop Science 2015; 55(4): 1741-1748.
65. Miwa K., Fujiwara T. Boron transport in plants: co-ordinated regulation of transporters. Annals of Botany 2010; 105: 1103-1108.
66. Miwa K., Takano J., Omori H., Seki M., Shinozaki K., Fujiwara T. Plants tolerant of high boron levels. Science 2007; 318(5855): 1417.
67. Molassiotis A., Sotiropoulos T., Tanou G., Diamantidis G., Therios I. Boron-induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). Environmental and Experimental Botany 2006; 56: 54-62.
68. Nable RO., Banuelos GS., Paull JG. Boron toxicity. Plant and Soil 1997; 193: 191-189.
69. Naeem M., Naeem M., Ahmad R., Ahmad R., Ashraf M., Ihsan M., Nawaz F., Athar HR., Ashraf M., Abbas HT., Abdullah M. Improving drought tolerance in maize by foliar application of boron: water status, antioxidative defense and photosynthetic capacity. Archieves in Agronomy and Soil Science 2018; 64(5): 626-639.
70. Nozawa A., Takano J., Kobayashi M., Von Wiren N., Fujiwara T. Roles of BOR1, DUR3 and FPS1 in B transport and B tolerance in Saccharomyces cerevisiae. FEMS Microbiology Letters 2006; 262: 216-222.
71. O’Neil MA., Warrenfeltz D., Kates K., Pellerin P., Doco T., Darvill AG., Albersheim P. Rhamnogalatturonan-II, a pectic polysaccharide in the walls of growing plant cell, forms a dimmer that is covalently cross-linked by a borate ester. Journal of Biological Chemistry 1996; 271: 22923-22930.
72. O’Neill MA., Ishii T., Albersheim P., Darvill AG. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annual Review of Plant Biology 2004; 55: 109-139.
73. Ouzounidou G., Paschalidis C., Petropoulos D., Koriki A., Zamanidis P., Petridis A. Interaction of soil moisture and excess of boron and nitrogen on lettuce growth and quality. Horticultural Science 2013; 40(3): 119-125.
74. Özdemir M., Kıpçak İ. Recovery of boron from borax sludge of boron industry. Minerals Engineering 2010; 23: 685-690.
75. Pagliuso D., Pereira JPJ., Ulrich JC., Cotrim MEB., Buckeridge MS., Grandis A. Carbon allocation of Spirodela polyrhiza under boron toxicity. Frontiers in Plant Science 2023; 14: 1208888.
76. Pang Y., Li L., Ren F., Lu P., Wei P., Cai J., Xin L., Zhang J., Chen J., Wang X. Overexpression of the tonoplast aquaporin AtTIP5;1 conferred tolerance to boron toxicity in Arabidopsis. Journal of Genetics and Genomics 2010; 37: 389-397.
77. Papadakis IE., Tsiantas PI., Tsaniklidis G., Landi M., Psychoyou M., Fasseas C. Changes in sugar metabolism associated to stem bark thickening partially assist young tissues of Eriobotrya japonica seedlings under boron stress. Journal of Plant Physiology 2018; 231: 337-345.
78. Pereira GL., Siqueira JA., Batista-Silva W., Cardoso FB., Nunes-Nesi A., Araujo WL. Boron: More than an essential element for land plants. Frontiers in Plant Science 2021; 11: 610307.
79. Petersson F., Jonsson M. The reactivity of hydroxyl radicals toward boric acid as a function of pH. The Journal of Physical Chemistry A 2024; 128(36): 7593-7600.
80. Pye LD., Frechette VD., Kreidl NJ. Borate glasses: Structure, Properties, Applications. Part of the Materials Science and Research Book Series, MSR. 2012: Vol. 12, Springer Science & Business Media.
81. Qin S., Xu Y., Nie Z., Liu H., Gao W., Li C., Zhao P. Metabolomic and antioxidant enzyme activity changes in response to cadmium stress under boron application of wheat (Triticum aestivum). Enviromental Science and Pollution Research 2022; 29: 34701-34713.
82. Reid RJ., Hayes JE., Post A., Stangoulis JCR., Graham RD. A critical analysis of the causes of boron toxicity in plants. Plant Cell and Environment 2004; 25: 1405-1414.
83. Riaz M., Kamran M., El-Esawi MA., Hussain S., Wang X. Boron-toxicity induced changes in cell wall components, boron forms, and antioxidant defense system in rice seedlings. Ecotoxicology and Environmental Safety 2021; 216: 112192.
84. Rosa M., Prado C., Podazza G., Interdonato R., Gonzalez JA., Hilal M., Prado FE. Soluble sugars metabolism, sensing and abiotic stress. A complex network in the life of plants. Plant Signaling and Behavior 2009; 4: 388-393.
85. Sang W., Huang ZR., Qi YP., Yang LT., Guo P., Chen LS. An investigation of B-toxicity in leaves of two citrus species differing in boron-tolerance using comparative proteomics. Journal of Proteomics 2015; 123: 128-146.
86. Sarı D. Effects of PEG-induced drought stress and different boron levels on seed germination and seedling growth characteristics in chickpea (Cicer arietinum L.) and lentil (Lens culinaris Medik.). Türkiye Tarımsal Araştırmalar Dergisi 2023; 10(2): 154-161.
87. Schachtman DP., Shin R. Nutrient sensing and signaling: NPKS. Annual Review of Plant Biology 2007; 58: 47-69.
88. Shi Y., Huang C., Wang X., Jin W., Wang M., Yu H. Physiological and iTRAQ based quantitative proteomics analyses reveal the similarities and diferences in stress responses between short term boron deficiency and toxicity in wheat roots. Molecular Biology Reports 2023; 50: 3613632.
89. Singh P., Singh G., Dadrwal BK., Yadav N. Importance of boron for crops: A review. Frontiers in Crop Improvement 2021; 9: 2392-2402.
90. Sutton T., Baumann U., Hayes J., Collins NC., Shi BJ., Schnurbusch T., Hay A., Mayo G., Pallotta M., Tester M., Langridge P. Boron-toxicity tolerance in barley arising from efflux transporter amplification. Science 2007; 318: 1446-1449.
91. Takano J., Miwa K., Yuan L., von Wiren N., Fujiwara T. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proceeding of the National Academy of Science USA 2005; 102: 12276-12281.
92. Takano J., Noguchi K., Yasumori M., Kobayashi M., Gajdos Z., Miwa K., Hayashi H., Yoneyama T., Fujiwara T. Arabidopsis boron transporter for xylem loading. Nature 2002; 420: 282-283.
93. Takano J., Wada M., Ludewig U., Schaaf G., von Wiren N., Fujiwara T. The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. The Plant Cell 2006; 18: 1498-1509.
94. Tanaka M., Fujiwara T. Physiological roles and transport mechanism of boron. Perspectives from plants. Pflugers Archieve-European Journal of Physiology 2008; 456(4): 671-677.
95. Tanaka M., Takano J., Chiba Y., Lombardo F., Ogasawara Y., Onouchi H., Naito S., Fujiwara T. Boron dependent degradation of NIP5;1 mRNA for acclimation to excess boron conditions in Arabidopsis. Plant Cell 2011; 23: 3547-3559.
96. Tepe M., Aydemir T. Antioxidant responses of lentil and barley plants to boron toxicity under different nitrogen sources. African Journal of Biotechnology 2011; 53(10): 10882-10891.
97. Turan M., Taban N., Taban S. Effect of calcium on the alleviation of boron toxicity and localization of boron and calcium in cell wall of wheat. Notulae Botanicae Horticulture Agrobotanici Cluj-Napoca 2009; 37(2): 99-103.
98. Uluışık I., Karakaya HC., Koç A. The importance of boron in biological systems. Journal of Trace Elements in Medicine and Biology 2018; 45: 156-162.
99. Vera-Maldonado P., Aquea F., Reyes-Diaz M., Carcamo-Fincheira P., Soto-Cerda B., Nunes-Nesi A., Inostroza-Blancheteau C. Role of boron and its interaction with other elementsin plants. Frontiers in Plant Science 2024; 15: 1332459.
100. Voxeur A., Fry SC. Glycosylinositol phosphorylceramides from Rosa cell cultures are boron-bridged in the plasma membrane and form complexes with rhamnogalacturonan II. Plant Journal 2014; 79(1): 139-149.
101. Wimmer MA., Mühling KH., Lauchli A., Brown PH., Goldbach HE. The interaction between salinity and boron toxicity effects the subcellular distribution of ions and proteins in wheat leaves. Plant Cell and Environment 2003; 26: 1267-1274.
102. Xu S., He C., Zhao Y., Yang X., Xu H. Generalized octet rule with fractional occupancies for boron. Journal of the American Chemical Society 2023; 145(45): 25003-25009.
103. Yang LT., Pan JF., Hu NJ., Chen HH., Jiang HX., Lu YB., Chen LS. Citrus physiological and molecular response to boron stresses. Plants 2022; 11(1). 40.
104. Ye JY., Tian WH., Jin CW. Nitrogen in plants: from nutrition to the modulation of abiotic stress adaptation. Stress Biology 2022; 2: 4-18.
105. Zhang L., Suo L., Shan Y., Wang B. Glutathione alleviates boron toxicity by modulating nitrogen metabolism and boron uptake in rice seedlings. Türkish Journal of Agriculture and Forestry 2024; 48: 1011-1022.
106. Zhao S., Huq ME., Fahad S., Kamran M., Riaz M. Boron toxicity in plants: understanding mechanisms and developing coping strategies; a review. Plant Cell Reports 2024; 43: 238.
107. Zimicz CC., Moretto AS., Camilion C. Characterization of boron toxicity tolerance of two soybean (Glycine max L.) varieties. Journal of Soil Science and Plant Nutrition 2023; 23: 4101-4114.