Abstract
Boron is one of the micronutrients that mostly limits crop yield in Brazil, especially for tomato. When boron is deficient, there is initially growth reduction in meristematic tissues (root ends and branches), although for tomato, this behavior has not yet been characterized. The aim of this work was to characterize the effects of boron deficiency on biometric characteristics, anatomical changes and deficiency symptoms in cherry tomato plants. For this, cherry tomato plants of cultivar Sindy were cultivated in nutrient solution and submitted to two treatments: (1) complete nutrient solution; and (2) nutrient solution without boron. Sixty days after seedling transplanting, phytotechnical and anatomical characteristics of leaves, stems and roots were evaluated. Drastic anatomical changes were observed in plants deficient in boron, both in leaves and stems. Disorganized vascular bundle, as well as xylem and phloem, with atypical cellular composition was observed. The root development was also affected by boron deficiency showing elongation restriction and apical meristematic necrosis, which compromised the long distance transport in the plant. This affected mainly the inflorescence formation and consequently reduce the fruit production.
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References
Ahmad S, Akhtar LH, Iqbal N, Nasim M (2009) Cotton (Gossypium hirsutum L.) varieties responded differently to foliar applied boron in terms of quality and yield. Soil Environ 28:88–92
Araujo L, Lemos LMC, Silva KJP, Milagres CC, Cardoso DSCP, Alves LC, Pereira PRG (2013) Tomate cereja cultivado em diferentes concentrações de solução nutritiva no sistema hidropônico capilar. Unimontes Científica, Montes Claros 15:18–26
Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Biol 49:481–500. https://doi.org/10.1146/annurev.arplant.49.1.481
Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrients: micronutrients. In: Marschner P (ed) Marschner’s mineral nutrition of higher plants. Academic Press, Cambridge, pp 191–248
Brown PH, Hu H (1997) Does boron play only a structural role in growing tissues of higher plants? Plant Soil 196:211–215. https://doi.org/10.1023/A:1004245823080
Brown PH, Bellaloui N, Wimmer MA, Bassil ES, Ruiz J, Hu H, Pfeffer H, Dannel F, Römheld V (2002) Boron in plant biology. Plant Biol 4:205–223. https://doi.org/10.1055/s-2002-25740
Cakmak I, Römheld V (1997) Boron deficiency-induced impairments of cellular functions in plant. Plant Soil 193:71–83. https://doi.org/10.1023/A:1004259808322
Camacho-Cristóbal JJ, Rexach J, González-Fontes A (2008) Boron in plants: deficiency and toxicity. J Integr Plant Biol 50:1247–1255. https://doi.org/10.1111/j.1744-7909.2008.00742.x
Dell B, Huang L (1997) Physiological response of plants to low boron. Plant Soil 193:103–120. https://doi.org/10.1023/A:1004264009230
Dugger WM (1983) Boron in plant metabolism. In: Lauchli A, Bieleski RL (eds) Encyclopedia of plant physiology 15B. Springer, Berlin, pp 626–650
Fernandes AA, Martinez HEP, Fontes PCR (2002) Productivity, fruit quality and nutritional status of single truss long shelf life tomato, cultivated in hydroponic system, with different nutrient source. Hortic Bras 20:564–570
Goldbach HE (1997) A critical review on current hypotheses concerning the role of boron in higher plants: suggestions for further research and methodological requirements. J Trace Microprobe Technol 15:51–91
Goldbach HE, Wimmer MA (2007) Boron in plants and animals: is there a role beyond cell-wall structure. J Plant Nutr Soil Sci 170:39–48. https://doi.org/10.1002/jpln.200625161
Guidi L, Degl’Innocenti E, Carmassi G, Massa D, Pardossi A (2011) Effects of boron on leaf chlorophyll fluorescence of greenhouse tomato grown with saline water. Environ Exp Bot 73:57–63. https://doi.org/10.1016/j.envexpbot.2010.09.017
Han S, Chen LS, Jiang HX, Smith BR, Yang LT, **e CY (2008) Boron deficiency decreases growth and photosynthesis and increases starch and hexoses in leaves of citrus seedlings. J Plant Physiol 165:1331–1341. https://doi.org/10.1016/j.jplph.2007.11.002
Hu H, Brown PH (1994) Boron uptake by sunflower, squash and cultured tobacco cells. Physiol Plant 91:435–441. https://doi.org/10.1111/j.1399-3054.1994.tb02971.x
Huang JH, Cai ZJ, Wen SX, Guo P, Ye X, Lin GZ, Chen LS (2014) Effects of boron toxicity on root and leaf anatomy in two Citrus species differing in boron tolerance. Trees 28:1653–1666. https://doi.org/10.1007/s00468-014-1075-1
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York
Katyal JC, Singh B (1992) Availability of boron in the soil and its uptake by rice as influenced by soil moisture regimes. Oryza 29:384–387
Kouchi H, Kumazawa K (1975) Anatomical response of root tips to boron deficiency I. Effects of boron deficiency on elongation of root tips and their morphological characteristics. Soil Sci Plant Nutr 21:21–28. https://doi.org/10.1080/00380768.1975.10432617
Kouchi H, Kumazawa K (1976) Anatomical response of root tips to boron deficiency III. Effect of boron deficiency on sub-cellular structure of root tips, particularly on morphology of cell wall and its related organelles. Soil Sci Plant Nutr 22:53–71. https://doi.org/10.1080/00380768.1976.10432967
Li M, Zhao Z, Zhang Z, Zhang W, Zhou J, Xu F, Liu X (2017) Effect of boron deficiency on anatomical structure and chemical composition of petioles and photosynthesis of leaves in cotton (Gossypium hirsutum L.). Sci Rep 7:1–9. https://doi.org/10.1038/s41598-017-04655-z
Malavolta E, Vitti GC, Oliveira AS (1997) Avaliação do estado nutricional das plantas: princípios e aplicações, 2nd edn. Potafos, Piracicaba
Marschner H (2012) Mineral nutrition of higher plants, 3rd edn. Academic Press, London
Martello JM (2016) Boro em cana-de-açúcar cultivada em solução nutritiva. Dissertação apresentada à Faculdade de Ciências Agronômicas da UNESP
Matoh T, Ishigaki KI, Mizutani M, Matsunaga W, Takabe K (1992) Boron nutrition of cultured tobacco BY-2 cells. 1. Requirement for and intracellular localization of boron and selection of cells that tolerate low levels of boron. Plant Cell Physiol 33:1135–1141
Mengel K, Kirkby EA (2001) Principles of plant nutrition. Kluwer Academic Publishers, Dordrecht
Moraes-Dallaqua MA, Beltrati CM, Rodrigues JD (2000) Anatomia de ápices radiculares de feijão cv. Carioca submetidos a níveis de boro em solução nutritiva. Scientia Agricola 57:425–430. https://doi.org/10.1590/S0103-90162000000300009
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373. https://doi.org/10.1007/BF0124856
O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 249:846–849. https://doi.org/10.1126/science.1062319
O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139. https://doi.org/10.1146/annurev.arplant.55.031903.141750
Quaggio JA, Piza Junior CT (2001) Frutíferas tropicais. In: Ferreira ME, Cruz MCP, Raij B, Abreu CA (eds) Micronutrientes e elementos tóxicos na agricultura. CNPq/FAPESP/POTAFOS, Jaboticabal, pp 459–492
Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407. https://doi.org/10.1146/annurev-arplant-042811-105449
Zhao D, Oosterhuis DM (2002) Cotton carbon exchange, nonstructural carbohydrates, and boron distribution in tissues during development of boron deficiency. Field Crops Res 78:75–87. https://doi.org/10.1016/S0378-4290(02)00095-3
Zhou GF, Liu YZ, Sheng O, Wei QJ, Yang CQ, Peng SA (2015) Transcription profiles of boron-deficiency-responsive genes in citrus rootstock root by suppression subtractive hybridization and cDNA microarray. Front Plant Sci 795:1–15. https://doi.org/10.3389/fpls.2014.00795
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The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Finance Code 001) for financial support.
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CCM collected the literature, analyzed the data and wrote the manuscript; JTLSM have performed the experiment work; MCV and HEPM coordinated the study and contributed in the manuscript writing. All authors reviewed the manuscript.
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Milagres, C.C., Maia, J.T.L.S., Ventrella, M.C. et al. Anatomical changes in cherry tomato plants caused by boron deficiency. Braz. J. Bot 42, 319–328 (2019). https://doi.org/10.1007/s40415-019-00537-y
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DOI: https://doi.org/10.1007/s40415-019-00537-y