III.Heat stress in Triticum: kinetics of Na, K and P accumulation

RESEARCH ARTICLE

III.Heat stress in Triticum: kinetics of Na, K and P accumulation

Ana S. Dias^I,II,*; Ana L. Fernando^I,III; Fernando C. Lidon^I,III

^IGrupo de Disciplinas de Ecologia da Hidrosfera, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Quinta da Torre, 2829-516 Caparica, Portugal

^IIInstituto Nacional de Investigação Agrária, Instituto Nacional dos Recursos Biológicos, I.P., Estrada de Gil Vaz, Elvas, Portugal

^IIIUnidade de Biotecnologia Ambiental / FCT-UNL, 2829-516 Monte de Caparica, Portugal

ABSTRACT

Genotypes of bread and durum wheat were submitted to heat stress after anthesis and the accumulation of Na, K and P, at booting, grain filling and maturity, were investigated. It was found that, after anthesis, the levels of Na in shoots were considerably higher in durum relatively to bread wheat, being this trend also observed in the total plant accumulation. In these genotypes, heat stress affected significantly Na concentration in shoots. In general, heat stressed plants had significant higher levels of K in the shoots and the proportion of this nutrient translocation from the roots also increased with heat stress. In general, the levels of P didn't show significant differences with heat stress. The effects of heat stress among the wheat genotypes life cycle are characterized and discussed.

Key words:Triticum aestivum L.; Triticum turgidum subsp. Durum; heat stress; nutrients uptake, nutrients translocation.

INTRODUCTION

The optimal mean temperature for the crops growth cycle might vary between 15-18ºC (Chowdhury and Wardlaw 1978), being 20ºC the optimal value for grain filling (Dupont and Altenbach 2003; Russell and Wilson 1994). Moreover, the yield performance of wheat genotypes is strongly affected by heat stress (Spiertz 1977; Wardlaw et al. 2002), being pointed (Wardlaw et al. 1989) that a global reduction of about 3-4% occurs in crops production when the temperature increases by 1ºC (i.e., mean temperatures above optimum). Ciaffi et al. (1996) further indicated that, even short periods of high temperature (35-40ºC) during grain filling can have a negative effect on yield and quality.

Within plant tissues, the accumulation of K+ is required for pH stabilization of the cytoplasm, to increase the osmotic potential in the vacuoles (Marschner 1995), and to promote cellular growth which determines higher yields (Lindhauer 1983). The inorganic P can also stimulate plant growth, as it regulates carbon flux between starch and sucrose biosynthesis (Terry and Rao 1991; Usuda and Shimogawara 1991) and phosphate distribution of photosynthates among tissues (Qiu and Israel 1994; Rao and Terry 1989). Although Na is not essential for plant species (Subbarao et al. 1999; 2000) also stimulates plant growth (Subbarao et al. 2003; Takahashi and Maejima 1998) since it has a high capacity to exchange K+ (Subbarao et al., 2003). Nevertheless, as most plants have an high selectivity K+ uptake (in the interface soil/roots), and translocation to the shoots (Subbarao and Johansen, 2002), the levels of Na are relatively low in grains (Subbarao et al. 2000; Subbarao and Johansen 2002).

Working with two genotypes of Triticum aestivum (Sever from Portugal and Golia from Italy) and Triticum turgidum subsp. turgidum (TE 9306 from Portugal and Acalou from France), having different tolerance to high temperature after anthesis (Dias et al., 2008, 2009; Dias and Lidon 2009, Maçãs et al. 1999; 2000), an insight in the magnitude of the implications of heat stress on Na, K and P uptake (by the roots) and translocation to the shoots, is presented. The implications on K, P and Na accumulation in the roots, shoots and spikes are characterized, since these nutrients are linked to cellular growth, being therefore hypothesized that the yield of crops reduction associated to heat stress implicates significant changes of these nutrients roots uptake and shoots translocation kinetics.

MATERIALS AND METHODS

Plant material and growth conditions: Bread wheat (Triticum aestivum L., genotypes Sever and Golia) and durum wheat (Triticum turgidum subsp. durum, genotypes TE 9306 and Acalou) grains were washed in distilled water and sterilized by immersion in mercury dichloride solution (1:1000) for 2 minutes. The grains were next washed five times in deionizer water and placed in an oven at 28ºC for 24 hours. Immediately thereafter the seeds were grown in a greenhouse (under natural light, between March and May in Lisbon/Portugal - 38º 42' N; 9º 05' W; photoperiod varying between 12 and 14 hours) in 25 x 21 cm pots containing a 1:1 perlite and vermiculite mixture. The experiment was conducted using 136 pots. Half of these pots were putted under heat stress after anthesis. For each genotype 17 replicates were used (with and without heat stress). Ten seeds were grown per pot and two weeks later five were selected, being the others removed. Accordingly, 680 plants were used. In each plant all tillers were removed, keeping only the main culm. During all the experiment the position of the pots was changed weekly, to minimize the effects due to irradiance variations. Plants were irrigated weakly but alternatively with distillated water or with a standard nutrient solution, alternately (in ml/100L, starter/pre-anthesis/post-anthesis, Ca (NO₃)₂ 100/100/50; KNO₃ 50/200/100; KH₂PO₄ 100/100/100; MgSO₄ 200/200/100; K₂SiO₃ 100/100/0; Fe(NO₃)₃ 20/5/5; EDTA 25/5/5; MnCl₂ 5/10/5; ZnSO₄ 20/10/10; H₃BO₃ 10/5/2; CuSO₄ 5/5/3; Na₂MoO₄ 15/5/5). During the vegetative and reproductive growth, plants were kept under similar environment conditions. At anthesis, the plants were divided in two groups and submitted to two different temperature conditions (controlled and heat stress). Under heat stress the plants were submitted to temperatures that rose until 40ºC. During the grain filling period, control plants grew under regimes with mean temperatures (day/night) of 25/14ºC and 31/20ºC (control and heat stress conditions, respectively). The average of day/night temperatures was calculated as the mean readings of each two hours, during each 24 hours period.

Nutrients analysis: The concentrations of Na, K and P were determined in roots, shoots and spikes (at booting-69/70 days after anthesis; grain filling-108/109 and 109/112 days after anthesis, for the genotypes submitted to control and heat stress conditions, respectively). Five randomized plants of each genotype, from each heat treatment, were used for nutrients analysis. Plant samples were washed, the fresh weight was determined in each fraction and, therefore, dry weight was measured after dryness in an oven for 100ºC during 72h. For Na and K, one gram of dry material, from each sample, was mineralized through incineration at about 550ºC, and followed by nitric acid digestion (Vandecasteele and Block 1993). A Unicam model 939 absorption unit, equipped with a hollow cathode lamp was used for these metals determinations. For P concentrations determination, a hot digestion with HNO₃ and H₂SO₄ (Watts and Halliwell 1996) was carried out. Phosphates were determined by molecular absorption spectrophotometry (Cecil 9000 series), through formation of a chromophore with a solution of ammonium molibdato, in the presence of ascorbic acid and potassium tartarato and antimony (Watanabe and Olsen 1965). The mean concentration values of the nutrients and biomass yields of the roots, shoots and spikes (and grain weight) were used to determine the total related mean content in Triticum plants. The net uptake was determined adding these values. The mean of the translocation rates were obtained by calculating, on a percentage basis, the ratio between the means of these metal contents in the shoot and their net absorption.

Statistical analysis: Statistic analyses were performed with a two-way ANOVA (p<0.05), using STATISTICA, version 6 (2001), by StatSoft, Inc.

RESULTS AND DISCUSSION

From previous studies (Dias and Lidon 2009; Dias et al, 2008, 2009< Maçãs et al. 1999, 2000) it was found that Triticum aestivum L. genotype Sever is more tolerant to heat stress after anthesis than the genotype Golia and that Triticum turgidum subsp. durum genotype TE 9306 tolerance prevails relatively to the genotype Acalou (Dias and Lidon 2009; Dias et al, 2008, 2009). In this experiment, when these genotypes were submitted to heat stress after anthesis faced a consistent period of moderate high temperatures. Under these growth conditions, along the growth cycle, the levels of Na in the roots of the control plants remained similar in both plant species, but expressing different genome characteristics (Schachtman et al., 1991), in the shoots and spikes, were considerably higher in the durum wheat genotypes (Table 1). Although the ability to limit the accumulation of Na in leaves may be an important mechanism of salt tolerance because the excessive accumulation of Na causes the premature senescence of leaves (Schachtman and Munns, 1992), in the heat stressed species, during grain filling and at maturity, the levels of Na were higher in durum wheat. During grain filling, the levels of Na in the shoots of the durum wheat genotypes were 5 and 9 fold higher (relatively to bread wheat), in the control and heat stress treatments, respectively (Table 1). In Golia, during this growth phase, the concentrations of Na in the shoots decreased significantly (between control and heat stress conditions), but an opposite trend was found at maturity. In Sever significant differences could not be found (Table 1). During grain filling, in the Triticum durum genotypes, the contents of Na in the shoots also increased significantly, and in TE 9306 this trend persisted at maturity (Table 1). In both temperature treatments, the levels of Na in the spike of the durum wheat genotypes were 2 fold (in average) higher than those found for bread wheat genotypes (Table 1), being these patterns similar to those reported by Hussain et al. (2002). Nevertheless, in the spike, at maturity, the levels of Na decreased significantly in Sever, whereas an opposite trend occurred in Acalou (Table 1). As a general pattern, it was found that, during grain filling and at maturity, the higher levels of Na in the shoot of all the genotypes, comparatively to the spike (Table 1), agree with Watt and Merrill (1975), about the low mobilization of Na for the reproductive structures in wheat grain, additionally expressing a lower rate of Na accumulation independent of the growth of individual leaves and probably regulated by some root process, and a compartmentation within leaves, which enhances the ability to tolerate high concentrations of Na in leaves (Schachtman and Munns, 1992). During grain filling, the total accumulation of Na in the durum wheat genotypes was considerably higher relatively to the bread wheat genotypes, being this pattern mainly due to the shoot accumulation (Fig. 1). These data point an higher root Na absorption of durum wheat, coupled to an higher efficiency of its translocation to the shoots (Fig. 1), being the accumulation rates of Na in durum wheat superior (Table 2). During grain growth, the difference of Na accumulation between the Triticum species became more evident in Golia, since the proportion of Na translocated to the shoots was almost half of that found in the durum wheat genotypes (Fig. 1). Under heat stress, during grain filling, the total and shoot accumulation of Na in Acalou increased 29% and 34%, respectively, but in the end of this growth phase only an increase of 17% and 23% was found. During grain filling, this trend did not persist in TE 9306 (Fig. 1). However, in this genotype, this effect did not affect the levels of Na in the shoots, although might have decreased (non-significantly) the levels of Na in the spike (Table 1). At maturity, the accumulation trend found for both durum wheat genotypes was quite similar (Fig. 1).

In our study, as reported by Bergmann (1992), at booting, the contents of K in the shoots varied between 26-53 mg/g (Table 3), eventually displaying a close interaction with Na (Shirazi et al., 2005). It was also found that, as a general pattern, the concentrations of K in the control genotypes, decreased during the growth cycle in all tissues. This effect was similar to that reported by Lásztity (1987), with the additional K probably being involved in the regulation of cellular osmotic potential (Hsiao and Läuchli 1986). Under heat stress, it was found that the levels of K increased significantly: in the roots of Golia and TE 9306, during grain filling and at maturity, respectively; in the shoots of all genotypes (excepting Golia), during grain filling and at maturity, in Sever and TE 9306; in the spike of Acalou at maturity (Table 3). In the end of the growth cycle, total and shoot accumulation of K (thus, total uptake and the translocation rate) in the heat stressed Golia increased 14% and 20%, respectively (Fig. 2). In Acalou, during grain filling, total and shoot accumulation of K was also higher under heat stress conditions (Fig. 2), contributing to the significant effect of the high temperatures in the concentrations of K in the shoots, during grain filling and in the spike, at maturity (Table 3). Moreover, the decrease of the total amount of K accumulated in heat stressed plants of the genotype TE 9306 (Fig. 2), did not affect its shoot concentration.

At booting, the shoot contents of P varied between 2.6 - 3.1 mg/g (Table 4), values that are similar to those reported for Triticum in this growth phase (Bergmann 1992; Marschner 1995). As previously reported (Lásztity 1987) in the Triticum genotypes, the concentrations of P under controlled conditions decreased during all the growth cycle, following a close interaction with Na (Perveen et al., 2003), which eventually favored starch synthesis (Rijven and Gifford 1983; Walker 1980). Nevertheless, the levels of P in the spike remained higher comparatively to shoot levels (Table 4). As a general pattern, the levels of P in the shoot increased with high temperatures. This trend was also found for maize by Ashraf and Hafeez (2004). During grain filling, the contents of P increased significantly in the spike of Golia and in the roots of TE 9306 (Table 4). At maturity, a significant increase of P contents was found in the shoot of Golia and in the root of TE 9306 (Table 4). At maturity Sever, revealed a significant decrease of P contents, but the other genotypes showed an opposite trend (Table 4). In Acalou the levels of P didn't varied significantly during all the growth cycle (Table 4). The accumulation of P in the durum wheat genotypes showed only minor variations, but during grain growth, total and shoot accumulation of P was higher in heat stressed plants of Golia (Fig. 3). In this genotype, in the beginning of grain filling, the pronounced increase (46%) that occurred in the shoot accumulation of P (resulting of an high translocation from the roots) justified the significant increase of this nutrient concentration in the spike (Table 4). At the end of the growth cycle, the rate of total accumulation of P in the heat stressed plants of Sever was smaller comparatively to the control plants (Table 2). At maturity, this effect became evident in the decreased total and shoot accumulation of P (Fig. 3), which in conjunction with the absence of a significant variation (between temperature treatments) in its translocation to the shoot (Fig. 3) inhibited the contents (on a dry weight basis) in the shoots at the end of grain growth (Table 4).

In general it is concluded that although heat stress affected the root uptake and shoot translocation kinetics of Na, P and K, tolerance to this stress is not linked to a selective accumulation of Na, K and P in durum and bread wheat.

Schachtman DP, Munns R. (1992). Sodium accumulation in leaves of Triticum species that differ in salt tolerance. Functional Plant Biology 19: 331-340.

Received: 31 July 2009; Accepted 29 October 2009.

• Ashraf M, Hafeez M (2004) Thermotolerance of pearl millet and maize at early growth stages: growth and nutrient relations. Biol. Plant. 48:81-86.
• Bergmann W (1992) Nutritional disorders of plants: development, visual and analytical diagnosis. Gustav Fischer Verlag Jena, Stuttgart, New York
• Chowdhury SI, Wardlaw IF (1978) The effect of temperature on kernel development in cereals. Aust. J. Agric. Res. 29:205-223.
• Ciaffi M, Tozzi L, Borghi B, Corbellini M, Lafiandra E (1996) Effect of heat shock during grain filling on the gluten protein composition of bread wheat. J. Cereal Sci. 24:91-100.
• Dias AS, Bagulho AS, Lidon FC (2008). Ultrastructure and biochemical traits of bread and durum wheat grains under heat stress. Braz. J. Plant Physiol. 20: 323-333.
• Dias AS, Barreiro MG, Campos PS, Ramalho JC, Lidon FC (2009). Wheat dellular membrane thermotolerance under heat stress. J. Agron. Crop Sci. DOI: 10.1111/j.1439-037X.2009.00398.x.
• Dias AS, Lidon FC (2009). Evaluation of grain filling rate and duration in bread and durum wheat, under heat stress after anthesis. J. Agron. Crop Sci.,195: 137-147.
• Dupont FM, Altenbach SB (2003) Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. J. Cereal Sci. 38:133-146.
• Hsiao TC, Läuchli A (1986). Role of potassium in plant-water relations. In: Tinker B, Uuchli A (eds) Advances in Plant Nutrition, vol 2, pp. 281-312, New York.
• Hussain M, Naeem M, Ashraf MY, Iqbal Z (2002) Effect of NaCl salinity on growth and ion partitioning in some barley varieties. Online J. Biol. Sci. 2(9):608-611.
• Lásztity B (1987) The variation of element contents in triticale during vegetative growth. Nutr. Cycl. Agroecosyst. 13:155-159.
• Lindhauer MG (1983) Effect of potassium on water use efficiency. Proceedings 17^th Coll. Intern. Potash Inst., 81-97.
• Maçãs B, Gomes C, Dias, AS (1999) Efeito das temperaturas elevadas durante o enchimento do grão em trigo mole e rijo no Sul de Portugal. Melhoramento 36:27-45.
• Maçãs B, Gomes MC, Dias AS, Coutinho J (2000) The tolerance of durum wheat to high temperatures during grain filling. In: Royo C, Nachit MM, Di Fonzo N, Araus JL (eds) Durum wheat improvement in the Mediterranean region: new challenges. Options Méditerranéennes., pp 257-261, CIHEAM, Zaragoza, Espanha.
• Marschner H (1995) Mineral Nutrition of higher plants, 2^nd ed., pp 313-364, Academic Press London, UK.
• Perveen R, Wahid I, Naqvi II, Shaukat S (2003). Uptake and translocation of radioactive phosphorous in wheat (Triticum aestivum L.). Pakista J. Biol. Sci 6: 1966-1970.
• Qiu J, Israel DW (1994) Carbohydrate accumulation and utilization in soybean plants in response to altered phosphorus nutrition. Physiol. Plant. 90:722-728.
• Rao IM, Terry N (1989) Leaf Phosphate Status, Photosynthesis, and Carbon Partitioning in Sugar Beet I. Changes in Growth, Gas Exchange, and Calvin Cycle Enzymes I. Plant Physiol. 90:814-819.
• Rijven AHGC, Gifford RM (1983) Accumulation and conversion of sugars in developing wheat grains. 3. Non-diffusional uptake of sucrose, the substrate preferred by endosperm slices. Plant Cell Environ. 6:417-425.
• Russell G, Wilson GW (1994) An Agri-Pedo-Climatological Knowledge-Base of Wheat in Europe. Luxembourg: European Commission, Joint Research Centre.
• Schachtman DP, Munns R., Whitecross MI (1991). Variation in sodium exclusion and salt tolerance in Triticum tauschi Crop Sci. 31: 992-997.
• Shirazi MU, Ashraf MY, Khan MA, Naqvi MH (2005). Potassium induced salinity tolerance in wheat (Triticum aestivum L.). Int. J. Environm. Sci. Tech. 2: 233-236.
• Spiertz JHJ (1977) The influence of temperature and light intensity on grain growth in relation to the carbohydrate and nitrogen economy of the wheat plant. Neth. J. Agric. Sci. 25:182-197.
• Subbarao GV, Johansen C (2002) Physiological mechanisms relevant to genetic improvement of salinity tolerance in crop plants. In: Pessarakli M (ed.) Handbook of Plant and Crop Physiology, pp 857-880, Marcel Dekker Inc., New York.
• Subbarao GV, Ito O, Berry WL, Wheeler RM (2003) Sodium--A Functional Plant Nutrient. Crit. Rev. Plant Sci. 22: 391-416.
• Subbarao GV, Wheeler RM, Stutte GW (2000) Feasibility of substituting sodium for potassium in crop plants for advanced life support systems. Life Support and Biosphere Science 7:225-232.
• Subbarao GV, Wheeler RM, Stutte GW, Levine LH (1999) How far can sodium substitute for potassium in redbeet? J. Plant. Nutr. 22:1745-1761.
• Takahashi E, Maejima K (1998) Comparative research on sodium as a beneficial element for crop plants. Memoirs of the faculty of Agriculture of Kinki University VO, 57-72.
• Terry N, Rao IM (1991) Nutrients and photosynthesis: iron and phosphorus as case studies. In: Porter JR, Lawlor DW (eds), Plant Growth: Interactions with Nutrition and Environment, pp 55-79, Cambridge University Press, Cambridge, UK.
• Usuda H, Shimogawara K (1991) Phosphate deficiency in maize. II. Enzyme activities. Plant Cell Physiol 32:1313-1317
• Vandecasteele C, Block CB (1993) Modern methods for trace element determination. John Wiley & Sons, Chichester, UK.
• Walker DA (1980) Regulation of starch synthesis in leaves-the role of orthophosphate. In: Physiological Aspects of Crop Productivity. Proceedings of the 15th Colloquium of the International Potash Institute, pp. 195-207, Bern.
• Wardlaw IF, Blumenthal C, Larroque O, Wrigley CW (2002) Contrasting effects of chronic heat stress and heat shock on kernel weight and flour quality in wheat. Funct. Plant Biol. 29:25-34.
• Wardlaw IF, Dawson IA, Munibi P, Fewster R (1989) The tolerance of wheat to high temperatures during reproductive growth. I. Survey procedures and general response patterns. Aust. J. Agric. Res. 40:1-13.
• Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from the soil. Soil Sci. Soc. Am. Proc. 29:677-678.
• Watt BK, Merrill AL (1975) Composition of Foods.Handbook, No. 8. USDA.
• Watts S, Halliwell L (1996) Appendix 3 - Detailed field and chemical methods for soil. In: Watts S, Halliwell L (eds) Essential environmental Science, methods & techniques, pp 475-505, Routledge, London.

Publication Dates

• Publication in this collection
  21 May 2010
• Date of issue
  2009

History

• Accepted
  29 Oct 2009
• Received
  31 July 2009