The Impact of Sudden Low Temperature Stress of rRoot and Shoot on the Recovery of some of Vegetative and Physiological Traits of Tomato in the Presence of Boron

Document Type : Research Article

Authors

• F. Dezhabad
• M. Haghighi

Isfahan of Technology University

10.22067/jhorts4.v33i4.68996

Abstract

Introduction: Most plants, especially those that are native to hot areas, show signs of injury when exposed to low temperatures. Damages caused by cold stress occurs at the cell and organs level, which reflects it at the plant surface. Color change, chlorosis, general reduction of growth, cellular tissue destruction, non-absorption of nutrients, reduction of photosynthesis, non-transferring photosynthetic materials are from early effects of cold stress. Cellular responses to colds including loss of thoracic pressure, vacuolization, collapse of cytoplasmic membrane balance, cytoplasmic flow loss, and general organ dysfunction. The susceptibility of the plant to frost is different depending on the type of plant, variety, tissue morphology and other cellular characteristics, as well as the cold conditions of the period, time and cold intensity. In addition, it seems that organs of the plant have different degrees of cold tolerance. If the temperature of the aerial part is favorable, the low temperature of the root zone can be one of the factors limiting the root system and plant growth. The consumption of balanced boron content by neutralizing the negative effects of cold stress and mechanisms such as maintaining the structure of the membrane, improving and increasing root growth, increasing the synthesis of proteins needed for the plant, adjustment of stomatal movements and improved stomatal conductance, increased cell division, increased nitrogen metabolism and chlorophyll production, and its consequence was increased photosynthesis and dry matter production, increased activity of antioxidants, calcium / potassium ratio adjustment, optimizing the transfer of calcium in the plant, adjusting the amount of water and conducting it in the cell, increasing the moisture content and relative content of leaf water, transferring soluble materials and increasing water use efficiency creates a relative resistance to low temperature stress. Although the root temperature is very effective in plant growth, it has been less attractive. Therefore, the aim of this study was to investigate the effect of low temperature of root and shoot on the ability to restore plant growth and physiological activity in the presence and absence of boron.
Materials and Methods: In order to compare the impact of sudden low temperature stress of root and shoot on recovery of vegetative and physiological traits of tomato, a research was conducted in two separate experiments under controlled conditions in the greenhouse of Faculty of Agriculture, Isfahan University of Technology. Two experiments were factorial based on completely randomized design with 10 replications including two concentrations of boron (0, 0.5, 1 and 1.5 in ppm) and two temperature levels of shoot and root sections (10 degrees’ Celsius temperature, and 11 rootstock temperatures and 22 ° C optimum and control temperatures). Indicators included photosynthesis rate, respiration rate, stomatal carbon dioxide, stomatal conductance, chlorophyll fluorescence, chlorophyll index, water use efficiency, proline, antioxidant, phenol secretion from root and leaf extracts, leaf relative water content, soluble protein concentration, ion leakage, leaf water potential, root and shoot dry weights and starch content. Finally, the analysis of the results was done by statistical software statistic and comparing the meanings by LSD test at 5% level.
Result and discussion: The results showed that the highest amount of photosynthesis, root dry weight and dry weight of the aerial part were in the consumption of 0.5 ppm of boron during abrupt stresses of low temperature on the root after the recovery period. The highest amount of stem proline and electrolyte leakage were also obtained from 0.5-1.5 ppm of boron consumption during abrupt low temperature on the shoot part. According to the results, it was found that when stress has entered from the root zone to the aerial part of the plant, the plant was in the better conditions after the recovery period. It seems that when a cold stress occurred on the roots, the plant can produced more antioxidant substances, including phenol and proline, while counteracting the relative water content of the leaves were more effective with radical agents. Thus, in normal conditions, the roots of the plant operated at a lower temperature than the airspace. They also exhibited more adaptations to the lower air at the lower temperature than the air section and the plant is less damaged. At levels above the boron element due to the effect of boron toxicity and the production of excess free oxygen radicals, the plant probably suffered more severe damage than cold damage.
Conclusions: Sudden low temperatures stresses on the root and shoot had negative effects on the recovery of the vegetative and physiological traits of tomatoes. When lower temperatures were imposed on the shoot, the plant suffered much more damages. Consumption of 0.5 ppm of boron during cold stress by creating optimal conditions for growth also caused the relative neutralization.

Keywords

• Proline
• Photosynthesis
• Electrolyte leakage
• Root dry weight
• Shoot dry weight

20.1001.1.20084730.1398.33.4.3.5

---

References

1- Ahn S.J., Im Y.J., Chung G.C., Cho B.H., and Suh S.R. 1999. Physiological responses of grafted-cucumber leaves and rootstock roots affected by low root temperature. Plant Cell Reports, 19: 397-408.

2- Allen D.J., and Ort D.R. 2001. Impact of chilling temperature on photosynthesis in warm climate plants. Trends in Plant Science, 6: 36-42.

3- Ashraf M., and Foolad M.R. 2007. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environmental and Experimental Botany, 59: 206-216.

4- Azzarello E., Mugnai S., Pandolfi C., Masi E., Marone E., and Mancuso S. 2009. Comparing image (fractal analysis) and electrochemical (impedance spectroscopy and electrolyte leakage) techniques for the assessment of the freezing tolerance in olive, Trees 23:159-167.

5- Baba K., Itoh S., Hastings G., and Hoshina S. 1995. Photoinhibition of Photosystem I electron transfer activity in isolated Photosystem I preparations with different chlorophyll contents. Photosynthesis Research, 47: 121-130.

6- Bates L., Waldren R.P., and Teare I.D. 1973. Rapid determination of free proline for water-stress studies. Plant Soil, 39: 205-207.

7- Berry J.A., and Raison J.K. 1981. Response of macrophytes to temperature . Physiological Plant Ecology, 12:227-338.

8- Binzel M.L., Hasegawa P.M., Rhodes D., Handa S., Handa A.K., and Bressan R.A. 1987. Solute accumulation in tobacco cells adapted to NaCl. Plant Physiology, 84:1408-1415.

9- Blum B., and Ebercon A. 1981. Cell membrane stability as a measure of drought and heat tolerance in wheat. Journal of Crop Science, 21: 43- 47.

10- Bradford M.M. 1976. A rapid and sensitive method for quantitation of microgram of protein utilizing the principle of protein-dye binding. Analytical Biochemistry Quantities, 72: 248-254.

11- Cakmak I., and Römheld V. 1997. Boron deficiency-induced impairments of cellular functions in plants. Plant Soil, 193:71-83.

12- Camacho-Cristobal J.J., and Gonzalez-Fontes A. 2007. Boron deficiency decreases plasmalemma H+-ATPase expression and nitrate uptake, and promotes ammonium assimilation into asparagines in tobacco roots. Planta, 226:443-451.

13- Campos P.S., Quartin V., Ramalho J. C., and Nunes M.A. 2003. Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. Plants. Journal of Plant Physiology, 160: 283-292.

14- Chen Y., Zhang M., Chen T., Zhang Y., and An L. 2006. The relationship between seasonal changes in antioxidative system and freezing tolerance in the leaves of evergreen woody plants of Sabina. South Afrcan Journal of Botany, 72: 272-279.

15- Danon A., and Mayfield S. 1994. Light-regulated translation of chloroplast messenger RNAs through redox potential. Science, 266:1717–1719.

16- Deepah N., Kura C., singhb H., And Kapoor H.C. 2007. Antioxidant properties in sweet pepper (Capsicum annum L.) genoryps during maturation. Food Science Technology, 40: 121-124.

17- Eraslan F., Lnal A., Gunes A., and Alpaslan M. 2007. Boron toxicity alters nitrate reductase activity, proline accumulation, membrane permeability and mineral constituents of tomato and pepper plants. Journal of Plant Nutrition, 30(6):981-994.

18- Fox J., Del Pozo-Insfrica A.D., Hee Lee J., Sargent S.A., and Talcott S. T. 2005. Ripening induced chemical and antioxidant changes in bell pepper as affect harvest maturity and postharvest ethylene exposure. Horticultural Science, 40:732-736.

19- Gheybi M., and Malakooti J. 2004. A guide for wheat, nutrient deficiency and plant nutrition. Ministry of Agriculture Publishing.

20- Guertal E.A. 2004. Boron fertilization of bentagrass. Crop Science, 44: 204–208.

21- Guidong L., Cuncang J., and Yunhua W. 2011. Distribution of boron and its forms in young ‘‘Newhall’’ navel orange (Citrus sinensis Osb.) plants grafted on two rootstocks in response to deficient and excessive boron. Soil Science Plant Nutrition, 57: 93-104.

22- Haghighi M., Heidarian S., Teixeira J., and Silva da A. 2012. The effect of Titanium amendment in N-withholding nutrient solution on physiological and photosynthesis attributes and micro-nutrient uptake of tomato. Biological Trace Element Research, 150: 381-390.

23- Hasanfard A., Nezami A, and Nabati J. 2015. Importance of plant selection for cold tolerance. Fourth International Conference on Applied Research in Agricultural Science. (in Persian)

24- Hu Y., Zhu Z., Yang J. Ni X., and Zhu B. 2009. Grafting increase the salt tolerance of tomato by improvement of photosynthesis and enhancement of antioxidant enzymes activity Environmental and Experimental Botany, 66:270-278.

25- Irigoyen J.J., Emerrich D.W., and Sanchez-Diaz M. 1992. Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa plant. Physiological Plant, 84: 55-60.

26- Joshi S.C., Chandra S., and Palni L.M.S. 2007. Differences in photosynthetic characteristics and accumulation of osmoprotectants in saplings of evergreen plants grown inside and outside a glasshouse during the winter season. Photosynthetica, 45(4): 594-600.

27- Koichi M., Shigemi T., Toshihiko M., and Kazuyoshi K. 2005. Recovery responses of photosynthesis, transpiration, and stomatal conductance in kidney bean following drought stress. Environment of Experiment Botany, 53:205-214.

28- Koocheki A., Zand A., Rezvani Moghaddam P., Mahdavi Damghani A., Jami AL-Ahmadi M., and Vesal S. 2005. Plant Ecophysiology. Ferdowsi University of Mashhad Publication. (In Persian)

29- Liu P. 2001. The research development of molybdenum and boron nutrition in soybean. China Agricultural Science Bulletin, 17: 41–44

30- Lone M.I., Kueh J.S.H., Wyn Jones R.G., and Bright S.W.J. 1987. Influence of proline and glycinebetaine on salt tolerance of cultured barley embryos. Journal of Experimental Botany, 38:479-490.

31- Lyons M.J., Graham D., and Raison J.K. 1979. Low temperature stress in crop plants: The role of the membrane. Academic press, New York.

32- Malakooti M., and Tehrani M.M. 1999. The role of micronutrients in improving performance and improving product quality. Tarbiat Modares University Press. (in Persian)

33- Marschner H. 1995. Mineral Nutrition of Higher Plants (2nd Edition). Academic Press institute, London.

34- Molla S., Villar-Salvador P., Garcia-Fayos P., and Rubira J.L. 2006. Physiological and transplanting performance of holm oak seedlings grown in nurseries with different winter conditions. Forest Ecology and Management, 237: 218-226.

35- Mordi talavat M.M., Kazemi Z., and Siaadat S.A. 2016. Canola physiological, growth and yield response to boron application affected by heat stress due to late planting dates. Behzeraee keshavarzi, 18(1): 55-67.

36- Nasef M.A., Badran N.M., and Abd El-Hamide A.F. 2006. Response of peanut to foliar spray with boron and/or rhizobium inoculation. Journal of Applied Sciences Research, 2(12): 1330-1337.

37- O’Neil M.A., Ishii T., Albersheim P., and Darvil A.G. 2004. Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annual Review of Plant Biology, 55: 109-139.

38- Ort D.R. 2002. Chilling-induced limitations on photosynthesis in warm climate plants: contrasting mechanisms. Environmental Control in Biology, 40: 7-18.

39- Ouzounidou G., Ilias I., Kabataidid M., and Chatzimichail A. 2003. Comparative study of nutrient deficiencies on growth and photochemistry of tobacco. Journal of Plant Nutrition, 26: 1605-1616.

40- Quick P., Siegl G., Neuhaus E., and Feil R. 1989. Short term water stress leads to a stimulation of sucrose synthesis by activating sucrose phosphate synthase. Planta, 177: 535-546.

41- Rab A., and Saltveit M.E. 1996. Differential chilling sensitivity in cucumber seedling. Physiologia Plantarum, 96: 375-382.

42- Reid R.J., Hayes J.E., Post A., Stangoulis J.C.R., and Graham R.D. 2004. A critical analysis of the cause of boron toxicity in plants. Plant, Cell and Environment, 25:1405- 1414.

43- Ritchie S.W., Nyvgen H.I., and Halady A.S. 1990. Leaf water content and gas exchange parameters of two wheat genotypes differing in drought resistance. Crop Science, 30:105-111.

44- Romero P., Navarro J. M., Garcia F., and Ordaz P.B. 2004. Effects of regulated deficit irrigation during the pre-harvest period on gas exchange, leaf development and crop yield of mature almond trees. Tree Physiology, 24:303–312.

45- Saadatmand M., and Enteshari S. 2013. Effect of pre-treatment pre-treatment time with silicon on salinity tolerance in Iranian bovine herb (Echium amoenum Fisch & C.A. mey) Science and technology of greenhouse crops, 3(12):45-56.

46- Seppanen M.M. 2000. Characterize of freezing tolerance in Solanum commersonii with special reference of the relationship between and oxidative stress. Section of Crop Husbandry, 56: 4-44.

47- Sheligl H.Q. 1986. Die verwertung orgngischer souren durch chlorella lincht. Planta Journal, 47-51.

48- Shimono H., Hasegawa T., Fujimura S., and Iwama K. 2004. Responses of leaf photosynthesis and plant water status in rice to low water tempreture at different growth stage. Field Crop Research, 89: 71-83.

49- Sing R. P., Chidambara Murthy K. N., and Jayaprakash G.K. 2002. Studies on the antioxidant activity of pomegranate peel and seed extracts using in vitro models. Agricultural and Food Chemistry, 50: 81–86.

50- Sotiropoulos T.E., Therios I.N., Dimassi K.N., Bosabalidis A., and Kofidis G. 2002. Nutritional status, growth, CO2 assimilation, and leaf anatomical responses in two kiwifruit species under boron toxicity. Journal of Plant Nutrition, 25: 1249-1261.

51- Souza R. P., Machado Silva E.C., Lagoa J.A.B., and Silveria J.A.G. 2004. Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environmental and Experimental Botany, 51:45–56.

52- Taiz L., and Zeiger E. 2002. Plant Physiology Sunderland: (3ed). Sinauer Associates, Inctitute.

53- Tarigholeslami M., Kafi M., Nezami A., and Zarghami R. 2015. Effects of chilling stress on physiological and biochemical traits of three hybrid of Corn (Zea mays L.) in seedling stage. Journal of Plant Research, 29(3): 552-540.( in Persian with English abstract)

54- Tjus S.E., Møller B.L., Scheller H.V.1998. Photosystem I is an early target of photoinhibiton in barley illuminated at chilling temperatures. Plant Physiology, 116: 755-764.

55- Voetberg G.S., and Sharp R.E.1991. Growth of the maize primary root tip at low water potentials. III. Role of increased proline deposition in osmotic adjustment. Plant Physiology, 96:1125-1130.

56- Wyatt S.E., Rashotte A.M., Shipp M.J., Robertson D., and Muday G.K. 2002. Mutations in the gravity persistence signal loci in Arabidopsis disrupt the perception and/or signal transduction of gravitropic stimuli. Plant Physiology, 130(3):1426-1435.

57- Yu L., Haley S., Perret J., Harris M., andQian M.J. 2002. Free radical scavenging properties of wheat extracts. Agricultural and Food Chemistry, 50:1619–16.

58- Zhao D.Y., Shen L., Fan B., Liu K.L., Yu M.M., Zheng Y., Ding Y., and Sheng J.P. 2009. Physiological and genetic properties of tomato fruits from 2 cultivars differing in chilling tolerance at cold storage. Food Chemical, 74: 348–352.