Growth, yield and sugar content of potato tubers at different physiological ages

Crecimiento, rendimiento y contenido de azúcares a diferente edad fisiológica del tubérculo de papa

Sigfrido David Morales-Fernández^1*; Rafael Mora-Aguilar²; Yolanda Salinas-Moreno³; Juan Enrique Rodríguez-Pérez²; María Teresa Colinas-León²; Héctor Lozoya-Saldaña²

¹ Universidad Tecnológica de la Selva. Departamento de Investigación y Desarrollo. Carretera Ocosingo - Altamirano km 0.5, Ocosingo, Chiapas, C. P. 29950, MÉXICO. Correo-e: moralesuno1@hotmail.com, teléfono: 9191163799 (*Autor para correspondencia).

³ Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias. Centro - Altos de Jalisco. Carretera Tepatitlán - Lagos de Moreno km 8, colonia Rancho las Cruces, Tepatitlán de Morelos, Jalisco, C.P. 47600, MÉXICO.

Received: June 27, 2014.
Accepted: July 1, 2015.

Abstract

Potato tuber sugar content is an indicator of management conditions during crop growth, since it affects the degree of maturity, quality and sprouting. In this study, potato growth and yield under field conditions were assessed. Soluble sugar content in tubers at different physiological ages was determined, as was the effect these sugars have on seed-tuber sprouting during storage. To this end, four tuber samplings were carried out in four potato cultivars: one during tuber dormancy and three at different physiological ages. Determinations were made using high-performance liquid chromatography (HPLC). The variety Alpha had the longest biological cycle among all genotypes, and its yield was similar to that of the varieties Gigant and Vivaldi (659 g), which had yields 58 % greater than that of the variety Atlantic. Potato tubers with the physiological age of apical dominance (109 days after harvest, DAH), multiple sprouting (153 DAH) and senescence (237 DAH) had the highest sucrose, glucose and fructose contents (7.10 to 7.89 mg·g^-1), and the variety Vivaldi had the highest amount of sucrose and reducing and total sugars. The length and dry weight of the potato sprout showed a high positive and significant association with the content of reducing and total sugars.

Keywords: Solanum tuberosum L., phenology, tuber weight, soluble sugars, sprouting.

El contenido de azúcares en el tubérculo de papa permite conocer las condiciones de manejo durante el crecimiento del cultivo; el grado de madurez, la calidad y su efecto en la brotación. En la presente investigación se evaluó el crecimiento y rendimiento de papa en condiciones de campo. Se determinó el contenido de azúcares solubles de tubérculos en diferentes edades fisiológicas, así como el efecto que tienen en la brotación de semilla-tubérculo durante su almacenamiento. Para ello, en cuatro cultivares de papa se realizaron cuatro muestreos de tubérculo: uno durante el reposo y tres en diferentes edades fisiológicas. Las determinaciones se realizaron mediante cromatografía líquida de alta resolución (HPLC). La variedad Alpha tuvo el ciclo biológico más largo entre todos los genotipos, y su rendimiento fue similar al de Gigant y Vivaldi (659 g) quienes resultaron 58 % mayor que Atlantic. En los tubérculos de papa, con edad fisiológica de dominancia apical (109 días después de la cosecha, DDC), brotación múltiple (153 DDC) y senectud (237 DDC), fue donde se presentaron los mayores contenidos de sacarosa, glucosa y fructosa (7.10 a 7.89 mg·g^-1), y en los que Vivaldi registró la mayor cantidad de sacarosa, azúcares reductores y totales. La longitud y peso seco del brote de papa presentaron alta asociación positiva y significativa con el contenido de azúcares reductores y totales.

Palabras clave: Solanum tuberosum L., fenología, peso de tubérculos, azúcares solubles, brotación.

INTRODUCTION

The potato (Solanum tuberosum L.) is the fourth most important crop in the world (Sonnewald & Sonnewald, 2014). Tuber formation depends on, among other factors, the availability of assimilates and the ability of tubers to accumulate them. At the start of crop development, photoassimilates are mainly directed towards the development of leaves, stems and roots. However, this behavior changes with tuber initiation and growth because they increase the demand for assimilates (Wolf, 1993), and, consequently, the carbohydrates produced in the leaves throughout the crop cycle are translocated to tuber structures.

During tuber initiation, starch content is low but that of sugars is high, since the rate of transport of sugars produced in the leaves exceeds the rate of conversion to starch. As a result, when the tuber reaches physiological maturity the maximum dry matter accumulation and minimum amount of sugars are obtained. The latter are the main source of energy for promoting respiration or obtaining metabolic energy and cellular biosynthesis (Stark & Love, 2003).

At harvest, potato tubers are dormant and will not sprout, even when placed in a favorable environment, due to internal conditions such as the hormonal balance of promoters and inhibitors. As storage time goes on, the amount of promoters increases and sprout growth begins (Suttle, 2004). In this context, tubers have three development stages: apical dominance, multiple sprouting and senescence. In the first, dormancy is broken and a single sprout develops at the apex of the tuber; in the second, several sprouts distributed throughout the tuber start their growth and the last is characterized by long, branched, thin and weak sprouts; also, turgor loss occurs in the tuber (Wiersema, 1985).

The amount of sucrose in potato tubers is associated with the crop's degree of chemical maturity and the type of processing to be performed after storage, while the concentration of reducing sugars (glucose and fructose) is associated with frying quality (Sabba et al., 2007). Sugar content in tubers can be affected by the variety, its growth stage and environmental factors (crop management) (Thompson, Love, Sowokinos, Thornton, & Shock, 2008).

At harvest, Van Es and Hartmans (1981) reported concentrations of 1.28 % total sugars and 0.55 % reducing sugars in potato tubers. In other studies, Rodríguez-Saona and Wrolstad (1997) reported values of 0.13 % sucrose, 0.04 % glucose and 0.03 % fructose, while Sabba et al. (2007) indicate values of 0.11 % sucrose and 0.05 % glucose in dormant tubers.

Therefore, the objective of this research was to assess the growth and yield of four potato varieties, and to determine the sugar content in tubers at different physiological ages and the effect these sugars have on seed-tuber sprouting.

MATERIALS AND METHODS

This research was conducted in the municipality of San Lorenzo Cuapiaxtla, Tlaxcala (19º 18' N, 97º 46' W and 2,410 masl), under irrigated conditions. The region's climate classification is C (Wo) (w) b (i') C (Wo) (García, 1988) and it has regosol-type soil.

Four varieties were evaluated: Alpha, Atlantic, Gigant and Vivaldi. At planting, minitubers of 16 to 28 mm in diameter, in a state of apical dominance, were used. The experimental unit consisted of a row of 5 m long and 0.90 m wide, with 0.25 m spacing between plants; in each row, 20 minitubers were deposited at a depth of 10 cm.

At planting, and 20 days after emergence, the minitubers were fertilized with the formula 250-60-350-91-63 (N, P, K, Ca and Mg). During the growing season it was spray irrigated according to crop water requirements. From emergence to tuber physiological maturity, the maximum and minimum air temperature (°C) was recorded with a Taylor^® model 5458 mercury thermometer; using these data, the mean temperature was obtained.

A randomized complete block experimental design with four replications was used, and the experimental unit consisted of four rows.

From emergence the number of growing degree-days (GDD) accumulated at the beginning of each phase, and during each phenological stage of the crop, was determined with the classical residual method and 6 °C base temperature (Cao & Tibbitts, 1995). The emergence phase (E) occurred when 50 % of the plants of each experimental unit had emerged. The stolon initiation (SI) phase began when the stolon appeared on the main stem. Tuber initiation or growth (T) was identified as the time at which the apex of the stolon thickened. Tuber physiological maturity (TM) was visually identified by the loss of the foliage's green color or onset of senescence.

The vegetative stage (VS) was considered as the time from emergence to the beginning of the stolon phase, during which shoot growth and root system establishment occur. The initial reproductive stage (RS 1) includes the interval between the onset of the stolon stage and tuberization, and is characterized by stolon generation and growth. The final reproductive stage (RS 2) runs from the beginning of tuberization to tuber physiological maturity, where tuber growth occurred (Morales-Fernández et al., 2011).

Storage conditions

At harvest, the tubers of four randomly-selected plants per experimental unit were placed in paper bags to be later stored in the laboratory with ambient light, under the temperature and relative humidity conditions shown in Table 1, until showing maximum sprout development. It was considered that the tubers contained in the paper bags left dormancy when in 50 of them the main sprout measured 4 ± 2 mm. Sprout length (mm) and dry weight (mg) were recorded in five tubers selected at random from the experimental unit during: apical dominance (a single sprout), multiple sprouting (more than one sprout) and senescence (more than one sprout and turgor loss in tubers). On each occasion the longest sprout was measured, and from multiple sprouting all sprouts were measured for dry weight.

Quantification of soluble carbohydrates by high-performance liquid chromatography (HPLC)

Sample collection

Four samplings were performed during the storage period; the first during dormancy and the other three during the physiological ages of apical dominance, multiple sprouting and senescence of the tuber of each variety. On each occasion a tuber contained in the paper bags was taken and a sample obtained from it, with two replications being made for the larger tubers. Average tuber weights for the sampling process ranged between 152 and 181 g (Table 2).

From the central part of each tuber, between the basal and apical end, a sample of 5 ± 1 g was extracted and placed in liquid nitrogen (-196 °C) until analysis.

The frozen tuber samples were individually ground in a blender with 20 mL of 70 % HPLC-grade ethanol and brought to boiling temperature for 5 min. The extract was decanted, and a second extraction was made from the residue with 10 mL of ethanol; at the end, the extracts were mixed. Subsequently, the extract was centrifuged for 15 min at 4000 x g in a HERLE model Z230A centrifuge (Labnet International, Inc. Edison, NJ. USA), filtered with Whatman No. 4 paper and mannitol was added at a concentration of 4 mg·mL^-1 as internal standard. Finally, the extract was gauged to 25 mL with the same kind of solvent used for the extraction.

Then 10 mL of the extract were taken and concentrated to dryness with reduced pressure and low temperature (40 °C) in a BUCHI R-215 rotary evaporator (Switzerland). The residue was resuspended in 2 mL of HPLC-grade water in order to pass it through a column containing ion-exchange resins, one basic (0.5 mL of Dowex - 1 x 8 - Fluka) and the other acidic (0.5 mL of Dowex - 50W X8 - Fluka) at a ratio of 1:1 (w/w). The purified sample was passed through a 0.45-μm nylon acrodisc in order to collect the sample in a 1.5 mL vial.

HPLC sugar analysis

A Perkin Elmer series 200 high-performance liquid chromatography system (Boston Ma. USA), consisting of an autosampler, quaternary pump, degasser, refractive index detector and a column oven, was used. The system is operated with TotalChrom version 6.2.1 software. A Rezex RCM-monosaccharide Ca⁺² (8 %) column, 30 cm in length and 7.8 mm in diameter, was used. As the mobile phase, HPLC-grade water was used. The flow rate was 0.6 mL·min^-1, the sample injection volume 20 μL and the running time 25 min. Column temperature was maintained at 85 °C. Pattern curves were prepared using commercial sucrose, glucose and fructose standards (Sigma, MN), at concentrations of 0.5, 1.0, 2.5 and 5 mg·mL^-1 (Rodríguez-Saona & Wrolstad, 1997). At each point of the curves it was injected at least three times to obtain the data of the area associated with each concentration area; using this information, the regression equations for each sugar were obtained.

Analyses of variance and regression were performed with the data obtained. Also, Tukey's test was applied using the Statistical Analysis System package (SAS, 2004).

RESULTS AND DISCUSSION

Temperature

The mean temperature was 19 °C, similar to that reported by Cao and Tibbitts (1994) to obtain high biomass and tuber production (20 °C). Struik, Haverkort, Vreugdengil, Bus, and Dankert (1990) stress the importance of high temperatures during RS 1, as they promote stolon branching, an important condition for yield because the number of tubers formed is closely related to the number of stolons (Haverkort, Van De Waart, & Bodlaender, 1990).

Crop Phenology

In general, there were differential genotypic effects (P ≤ 0.05) in crop phenology. The variety Alpha required more GDD to reach the stolon (167), tuberization (261) and tuber physiological maturity (154) stages of the tuber; its life cycle was significantly longer than in the other varieties. Vivaldi was the variety that reached maturity the fastest, because it needed 15 % fewer GDD than Alpha (Table 3).

The vegetative and initial reproductive stages accounted for 45 % of the total duration of the crop cycle in Alpha, unlike the other varieties in which they accounted for only 26 %, while the final reproductive stage accounted for 55 % in Alpha and 74 % in the other varieties (Table 3). The greater precocity of Vivaldi, with respect to the other varieties, may be due to the lower GDD requirement in the vegetative and initial reproductive stages, because the shorter duration of these stages affects the crop growth period (Kooman, Fahem, Tegera, & Haverkort, 1996).

Yield and its components

Yield, expressed as total tuber weight per plant, was similar (P ≤ 0.05) in the varieties Alpha, Gigant and Vivaldi (659 g), which had a 58 % greater yield than the variety Atlantic (Table 4).

The components that contributed most to the yields of the varieties were: the number and weight of commercial and non-commercial tubers per plant, in the varieties Alpha and Vivaldi; and number, weight of commercial tubers per plant and average tuber weight per plant in Gigant. The variety Alpha had a significantly higher total number of tubers per plant, exceeding Atlantic by 60 % and Gigant and Vivaldi by 29 % (Table 4); however, it had a lower proportion of commercial tubers per plant (67 %) compared to the other varieties (72 %). This indicates that the increase in the number of tubers per plant might affect their final size (Walworth & Carling, 2002).

Sugar content in potato tubers

In general, the concentration of soluble sugars in tubers was higher during sprouting than dormancy, when they had, on average, 35, 39, 37 and 37 % lower sucrose, glucose, fructose and total sugar contents, respectively, than in tubers with a different physiological age (Table 5). These results agree with those reported by Sinha, Cash, and Chase (1992) and Sabba et al. (2007), who state that the least amount of sugars occurs during tuber dormancy, a situation that can be attributed, initially, to foliage senescence before harvest, and, consequently, a reduction in the transport of sugars and the conversion of them into starch in the tuber (Stark & Love, 2003).

As tubers left dormancy, their sugar content increased (P ≤ 0.05). Similar behavior was observed from apical dominance to tuber senescence (Table 5). In this regard, Sowokinos (2001) indicates that after tubers have been stored for prolonged periods they naturally experience increases in sugar content due to the conversion of starch into glucose and fructose. These changes are most evident when tubers are subjected to low temperatures, as occurred in November, December and January in the present study.

By analyzing the soluble sugars at dormancy and by tuber physiological age (Figure 2), it was found that the total sugar content was similar among varieties (P ≤ 0.05). However, the varieties Vivaldi and Gigant had a higher concentration of sucrose and glucose (28 and 29 % respectively), whereas Alpha and Gigant were 43 % higher in fructose (Figure 2a).

During apical dominance (Figure 2b), multiple sprouting (Figure 2c) and senescence (Figure 2d) of the tubers, the variety Vivaldi recorded the highest (P ≤ 0.05) amount of glucose, fructose and total sugars; moreover, in the apical dominance condition, it had 41 % higher sucrose content than the other varieties studied.

The interaction between varieties and tuber physiological age indicated that in soluble sugar content, Vivaldi had significantly greater variation through the physiological states (Table 6). In this respect, studies by Sowokinos (2001) indicate that the storage conditions and genetic load of the varieties may affect the sugar content in the tuber, as there are varieties that are more susceptible to the influence of environmental factors (Park et al., 2009; Pritchard & Adam, 1992).

The variety Alpha, at dormancy, had 67 % less sucrose than Vivaldi had in apical dominance, whereas the varieties Alpha, Atlantic and Vivaldi recorded 69 and 58 % less glucose and total sugars than Vivaldi in the other sprouting states. The variety Atlantic, at dormancy, was 77 % lower in fructose than Vivaldi in the senescence state (Table 6). These results coincide with those of Sinha et al. (1992), who obtained the least amount of sugars during tuber dormancy. This may be due to the ability of the genotypes to convert soluble sugars into starch (Stark & Love, 2003), coupled with decreased transport of sugars to the tuber due to senescence or foliage defoliation.

The variety Vivaldi recorded the highest sucrose (DA), glucose (BM and S), fructose (S) and total sugars (DA to S) contents among all varieties and physiological states (Table 6). Sowokinos (2001) indicates that tubers, after dormancy, experience an increase in sugar content due to the breakdown of starch into glucose and fructose; therefore, the tuber becomes a source of energy and substrates for subsequent processes (Vreugdenhil, 2004).

The appearance of the tuber sprout marks the end of dormancy (Suttle, 2004). From apical dominance until multiple sprouting of the tuber, the varieties Gigant and Vivaldi had significantly greater (P ≤ 0.05) sprout length (31 and 34 %) (Figure 3a) and dry weight (66 and 59 %) (Figure 3b), respectively, than the varieties Atlantic and Alpha. In senescent tubers, sprout length and dry weight reached the highest values. The varieties Gigant, Vivaldi and Atlantic had 34 % longer sprouts than Alpha. Gigant had 60 % higher sprout dry weight than Alpha and Atlantic (Figure 3).

Some research indicates that the diversification among varieties, in sprout length and dry matter, could be due to the length of the crop cycle because, during tuber sprouting, sprout length is shorter in late than early varieties (Knowles, Driskill, & Knowles, 2009), as occurred with the Alpha variety in the present study, which had the longest life cycle. Other studies attribute it to tuber size (Park et al., 2009) and the ability varieties have to breakdown the starch into reducing sugars, which are remobilized towards sprout formation and growth (Vreugdenhil, 2004).

Sugar content in the tuber sprouting process

During tuber sprouting, sprout length and dry weight had a high significant association with soluble sugar content (Figure 4). Increased sprout length (Figures 4a and 4b) and weight (Figures 4c and 4d) were accompanied by an increase, on average, in the concentration of reducing (glucose and fructose) and total sugars in apical dominance, multiple sprouting and senescence of the four varieties.

In the varieties Alpha (Figures 5a and 5b) and Gigant (Figures 5c and 5d), sprout length and weight increased as total sugars did; Vivaldi showed similar behavior in the content of reducing sugars (Figures 5e and 5f ).

Sugar content at harvest is one of the most important parameters that determine maturity and, during sprouting, sprout vigor in potato tubers (Ap Rees & Morrell, 1990). In the present study, the average behavior of varieties (Figure 4) and individually in Alpha, Gigant and Vivaldi (Figure 5) showed increased sprout length and dry weight during apical dominance, multiple sprouting and senescence as the content of reducing and total sugars increased. These results agree with those reported by Davies (1990) and Dogras et al. (1989), who during tuber sprouting recorded high reducing and total sugar contents, possibly due to the ability of some varieties to break down starch into glucose (Vreugdenhil, 2004), to be used as a source of energy and substrates for sprout development. Other studies indicate that when the potato tuber reaches maturity, the capacity for starch synthesis decreases, while the accumulation of sugars in the tuber increases, which contributes to the sprouting process (Viola et al., 2007), as occurred in this work.

In addition to sugars (Viola et al., 2007) and hormones (Sonnewald & Sonnewald, 2014), the genotype (Park et al., 2009), the degree of tuber maturity (Pritchard & Adam, 1992; Sabba et al., 2007) and temperatures during storage (Hertog, Tijskens, & Hak, 1997) can affect sprout growth.

In general, the content of sucrose and glucose, in all varieties studied, was always greater than that of fructose, results that agree with those reported by Rodríguez-Saona and Wrolstad (1997) during dormancy and those of Park et al. (2009) during tuber sprouting. This indicates the importance of these sugars, especially sucrose, which has been considered directly responsible for sprout growth (Debast et al., 2011).

CONCLUSIONS

The longer biological cycle of the potato variety Alpha did not result in greater total tuber weight per plant; since it had a similar behavior to that of Gigant and Vivaldi, where the number and weight of commercial tubers per plant were the components that contributed most to yield.

Physiological age (apical dominance, multiple sprouting and senescence) did not imply a higher concentration of soluble sugars in the tubers; in this regard, Vivaldi was the variety that showed the highest content of sucrose and reducing and total sugars.

A higher content of reducing and total sugars in the tuber resulted in greater sprout length and dry weight.

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