Influence of Air Temperature in the Emission of Nodes , Ramifications and Flowers in Hybrids of Watermelon ( Citrullus lanatus )

The culture of watermelon develops mainly under conditions of high temperature, being the temperature an element that directly affects the emission of vegetative and reproductive organs. There are no reports of the accumulation of temperature required for emission of branches, nodes and flowers. Thus, this experiment aimed to evaluate the rate of emission of vegetative and reproductive organs for hybrids of watermelon in relation to air temperature, using the hybrids of Manchester and Top Gun watermelons. The experiment was conducted in Federal University of Santa Maria, campus Frederico Westphalen-RS, from September to December 2014. Evaluations were conducted at every two days and it was determined the variables: nodes emission, final number of nodes on the main stem, number of primary and secondary ramifications and number of staminate flowers and open pistillate flowers related to accumulated thermal sum for the emission of such organs, and the ratio between the number of staminate flowers to the pistillate. The hybrids of watermelon present for plastochron of 18.8 °C node day, final number of nodes of the main ramification of 43 and number of primary and secondary ramifications of eight and 20, respectively. For the emission of staminate and pistillate flowers the hybrids need an accumulation 10.5 and 46.7 °C day, respectively. The number of staminate and pistillate flowers is 52 and nine, respectively, and the ration between flowers of 6.6:1.


Introduction
According to FAO (Food and Agriculture Organization), the largest watermelon [Citrullus lanatus (Thunb.)Matsum & Nakai] production is concentrated in China, accounting for 71% of the world production, followed by Turkey, Iran and Brazil.In Brazil, the watermelon culture presented an average production of 2 million tons in 2014 (FAOSTAT, 2015) and also has an important social role, being responsible for a large number of jobs, especially in the south, southeast, northeast and midwest regions (Souza et al., 2012).
Of the producing Brazilian states, Rio Grande do Sul (RS) is the largest producer and contributes about 20% of the national production, it has the largest cultivated area and the largest production in the country, surpassing 19 thousands hectares and about 433 thousand tons, respectively (IBGE, 2014).In RS the ideal climatic conditions occur between the months of September to March, when the average air temperature is about between 18 and 25 °C (Rezende et al., 2006).
For the species, one of the factors that most influence the cultivation is the air temperature, since it interferes directly in the plant development (Buozo & Kuchen, 2012).According to Lucas et al. (2012) for the watermelon cultivation the lower base temperature for nodes emission is 7.0 °C and the superior base temperature is 40 °C, with cardinal temperatures of 10 °C, 33 °C and 42 °C for the whole cycle (Trentin et al., 2008).Thus, the measurement of air temperature effect is an important tool used to estimate the period of plant development, through the accumulation of thermal units or degree-days above the base temperature estimated for the culture in study.
The accumulation of thermal units is validated to predict events like nodes and leaves emission, considering that the emission of these organs maintains a constant until the beginning of fruiting (Baker & Reddy, 2001).The time interval between the beginning of the formation of leaf primordia, morphological demonstration of apical growth and the development two internodes is called plastochron (Baker & Reddy, 2001).Thus, plastochron may be the most appropriate variable for understanding the influence of temperature on the physiology of the cultivation, considering the genotype of each species (Streck et al., 2005).
In addition to affecting the nodes emission, temperature directly affects the emission and development of ramifications (Nabinger, 2002).Watermelon presents primary and secondary ramifications (Dias & Rezende, 2010), and they are originated by cellular differentiation and proliferation of gems, activity caused, mainly, by decreasing dominance of apical meristem (Taiz & Zeiger, 2013).
Air temperature affects positively or negatively the emission and opening of the flowers, while temperatures above 40 °C harm the formation of watermelon flowers, both staminate and pistillate, causing abortion of flowers and pollen degradation, thus reducing impregnation of the pistillate flowers (Andrade Junior et al., 2007).For most species of cucurbits, the emission of flowers occurs due to the temperature and the ethylene (Salman-Minkov et al., 2008).The pistillate are the flowers with greater relevance for the crop, being emitted in smaller numbers, influencing the size and shape characteristics of the final fruit (Ulutürk, 2011).
The use of calendar days is a unit that does not reliably express the different periods of the plant development, therefore, for the emission of the first flower buds, the use of STa becomes effective, and, to the Crimson Sweet watermelon cultivar, the first flowers are emitted approximately 415 °C day (Trentin et al., 2008).
In ideal temperatures, the increasing number of open flowers occurs due to the rapid establishment of the plant, providing an increase in the production of photoassimilate, enabling the accumulation of reserves for the reproductive phase of the plant (Andrade Junior et al., 2007).Thus, the aim of this study was to determine the plastochron, final number of nodes in the main ramification, number of primary and secondary ramifications, flowers emission, number of staminate and pistillate flowers, as well as the ratio between staminate and pistillate flowers for hybrids of watermelon.

Method
The work was conducted in an experimental area of the Federal University of Santa Maria campus Frederico Westphalen-RS (Universidade Federal de Santa Maria campus Frederico Westphalen-RS), located at 27º23′48″ S, 53º25′45″ W, with an altitude of 490 m.According to Köppen climate classification, the weather is Cfa, and the predominant soil is the typic alumino-ferric Red Latossol (Embrapa, 1999).
The experimental design used was the randomized complete block using two hybrids of watermelon, with four replications.The experimental unit consisted of three rows of 46.5 meters, composed by the Manchester and Top Gun hybrids.Each block had two lateral rows as a border and the central row as a useful plot.In each replication 10 plants were selected just after the transplantation, which they were labeled, totaling the evaluation in 40 plants of each hybrid.The cultivars were chosen because they present similarities in their water requirement, nutrition, precocity, vigor and other agronomic characteristics.
The seeds were sown in September 2014 in plastic cups of 180 ml capacity, containing commercial substrate at peat basic.After sowing, the containers were placed in a greenhouse with a sprinkling irrigation system.
The preparation of the experimental area was initially constituted by desiccation and subsequent cropping of the area.Subsequently it was held a demarcation of the crop lines and, using a furrow attached to a tractor, the grooves were opened to the transplanting of the seedlings.The fertilization of the culture was held based in the soil analysis of the area, following the recommendation proposed by the Chemistry and Soil Fertility Commission to the states of Rio Grande do Sul and Santa Catarina (Comissão de Química e Fertilidade do Solo) (CQFSRS/SC, 2004).The transplant was carried out on October 8 th , 2014 manually spacing of 1.5 m between plants and 3.0 m between lines.Irrigation management was carried out via drip tap, based on crop evapotranspiration.
The meteorological data like minimum and maximum air temperature were collected from the automatic weather station belonging to the National Institute of Meteorology (Instituto Nacional de Meteorologia) (INMET), located about 330 m away from the experiment.
The variables used were: number of nodes, final number of nodes on the main stem, number of primary and secondary ramifications, number of staminate flowers and pistillate opened flowers.     is directly related the emission speed of vegetative organs of the culture, and it may accelerate or reduce the culture cycle, due to vegetative growth rate, such as emission of new leaves and stem elongation, actions occasioned by cell division in vegetative meristems and vascular tissue in the stem, subsequently paralyzed, occurring the senescence of the plant (Siqueira et al., 2001;Setiyono et al., 2007).It can positively or negatively act on the nodes emission process.Thus, temperatures above or below the optimal physiological cause reductions in plant growth, reducing expansion and cell division of plant tissues (Bahuguna & Jagadish, 2015).However, thermal stress can affect plant development, however, it does not restrict completely (Caron et al., 2003;Miranda & Júnior, 2010).Lucas et al. (2012) evaluating the Crimpson Sweet watermelon cultivar, have found an average value for plastochron of 23.3 °C day node -1 , values above those found in this experiment, and Manchester and Top Gun required 19.8 and 17.9 °C, showing that speed emission of a new node on the main stem of the hybrids require less temperature accumulation, justifying their precocity when compared to the cultivars.
In an experiment carried out with Crimson Sweet watermelon cultivar, Lucas et al. (2012) have reported the value of 34.2 nodes, presenting thus, a lower number of nodes in the main stem than what was found in this work.Trentin et al. (2008) working with the same cultivar, determined the accumulated thermal sum comprised between the emergence period until the beginning of flowering, from 417.3 °C day -1 .However, Lucas et al. (2012) related that the accumulated thermal sum for the same cultivar reached a value of approximately 760 °C day -1 between transplanting and the growth stoppage on the main stem.The same authors observed that the crop was affected when the air temperature exceeded the optimal range of 33 °C, thus reducing its growth.
The difference between this work compared to done by Trentin et al. (2008) with the Crimson Sweet cultivar where the thermal summation value was lower than that of hybrids, being justified by the assessment period in which the authors made the comments before the emission of the first flowers, differing from Lucas's work (2012), where the accumulated thermal sum was counted until the total stoppage period in the emission of nodes in the main stem, as realized in this experiment with hybrids.
The small differences observed between the characteristics of the evaluated hybrids can be justified by the endogenous conditions, related to physiological and morphological factors, such as the speed in cell division process, related to the air temperature (Nabinger, 2002).The same author reports that the air temperature directly affects the number of nodes and leaves, with the temperature rise above 30, but when it is considered day-degrees or daily thermal sum, leaf appearance speed on the stems becomes relatively constant.Explaining, thus, the least need for degree-days for the Manchester hybrid, causing it to emit higher number of secondary stems and may have to increase the production of photoassimilates, supplying the plant's needs.
The statistical equality between hybrids for all variables can be explained by the similarity of the hybrid cycle, since both are early considered, thus proving the efficiency of the method.In the literature, values for ramification emission for the watermelon culture are presented, such as Silva (2006), where it was done a work with 43 watermelon accessions, observing a range between the accessions, which were recorded the values of 3.7 to 13.7 ramifications of the first order.
The emission of primary ramifications from the main stem is another determining factor for the watermelon culture development, the need for thermal sum was 68 and 69 °C ramification -1 , to Manchester and Top Gun, respectively.For the emission of secondary ramification, the Manchester hybrid required approximately 18 °C and Top Gun 40 °C day for the emission of one ramification.With this emission, there is an increase in photosynthesizing area, increase in the emission of flowers located in the axillary gems, such in the main stem as in the primary and secondary ramifications (Boyhan et al., 2000).
Although no statistical differences, the Manchester hybrid emitted less primary ramifications and more secondary ramifications when compared to the Top Gun hybrid.This difference may be explained as a way to compensate for the least number of emitted primary ramifications, thereby increasing the photosynthesizing area.Works with reports of thermal sum for the emission of primary and secondary ramifications in watermelon or other Cucurbitaceae were not found.
The difference between the emission of primary and secondary ramification to the evaluated hybrids can be justified by the plant necessity in increasing the production of photoassimilates, and it is not possible to obtain them only with the photosynthetic area formed by the main stem and primary ramification.This difference can be justified due to the plants thermal perception, which can result in changes in the vegetative growth of hybrids (Bahuguna & Jagadish, 2015).
The anthesis of the first staminate flowers in watermelon culture, according to Costa et al. (2012) takes place between 35 and 40 days after emergence.Thus, these values do not express the action of environmental factors acting on the plant growth, making this information be on time in a certain place and cannot be applied to all of watermelon growing regions.
Depending on the final number of staminate flowers, for five cultivars of mini watermelons, Bomfim et al. (2012) had average values of 22.8 flowers plant -1 (HA-5161), 40.2 flowers plant -1 (Polimore), 43, 9 flowers plant -1 (HA-5106), 45.3 flowers plant -1 (HA-5158) 49.6 flowers and plant -1 (Minipérola).In this same study, average values of pistillate flowers per plant were checked, which ranged from 1.5 flowers (Polimore), 2.2 flowers (HA-5161), 2.7 flowers (Minipérola), 5.32 flowers (HA-5106) and 7.8 flowers (BOMFIM et al., 2012).The values are higher than those verified by Bomfim et al. (2012), both female and male flowers.For this variable, it is believed that is a characteristic linked directly to the plant genotype, having strong influence because it is related to the number of fertilized flowers, which may give rise to a fruit.
Studies of other cultures prove that the air temperature influences the flower anthesis, both complete or unisexual flowers, such as in Zea mays (Lima et al., 2008) and in Gladiolus × grandiflorus (Streck et al., 2012).The accumulated thermal sum also reported as thermal constant, has been widely used to determine the time necessary to the anthesis of flowers in various vegetables (Volpe et al., 2002).In general, for the emission of pistillate flowers it is necessary higher accumulation of thermal units than for staminate flowers, due to the fact of emitting fewer flowers, and their relationship is of great importance.
In a research done with four watermelon cultivars, the proportion of staminate flowers and pistillate flowers showed average results of 13.3:1 (Super Charleston) 13.4:1 (Elisa), 14.6:1 (Super Crimson) and 24:1 (Congo) (Duarte et al., 2015).Data obtained with the Crimson Sweet cultivar, the proportion of values between the two types of flowers was 5.5:1 (Souza & Malerbo-Souza, 2005).The values found in this experiment are lower than those observed by Duarte et al. (2015) and higher than Souza and Malerbo-Souza ( 2005), with 6.7 and 6.4:1 staminate/pistillate to Manchester and Top Gun, respectively.In watermelons, the ratio between the emission of staminate and pistillate flowers on the stem and ramifications is equivalent from four to 15 staminate flowers emitted in the leaf axils to the emission of a pistillate flower, and this feature depends on genetic factors (Salman-Minkov et al., 2008).
In low light conditions, reconciled at mild temperatures, there are higher emission of female flowers, whereas in conditions of days with high temperatures provides greater emission of male flowers (Wehner, 2016).Usually, there are more staminate flowers in relation to pistillate ones, and this relationship tends to be more evident when the temperatures are higher (Nicodemo et al., 2012).This characteristic is also found in other cucurbits such as melons with values of 6.1:1 to 11.3:1 (Crisóstomo et al., 2004), cucumber with values of 3.5:1 to 4.2:1 (Diola et al., 2008) and squash with a value of 2.3:1 (Nicodemo et al., 2007).Ethylene is the main regulator in the transition between male and female phases in the development and in the number of pistillate flowers per plant to different species of the cucurbits family (Silva et al., 2014;Salman-Minkov et al., 2008).
The largest number of staminate flowers in watermelon and also in other cucurbits is extremely important, because these plants are cross-pollination, and due to adhesion characteristics of pollen grains to the stamens, insects are necessary to carry out the collection thereof, for further fertilization of pistillate flowers, it is of fundamental importance this greater proportion between the two types of flowers.It is known that the air temperature directly influences flowering cucurbits, however, there were as yet no data in the literature regarding the number of thermal units required for the emission of primary and secondary ramifications, as well as the emission of pistillate and staminate, making the data obtained in this experiment innovative.
All the objectives established in this work were achieved.The Manchester and Top Gun watermelon hybrids are similar in vegetative and reproductive characteristics.The watermelon hybrids have an average plastochron of 18.8 °C nodes day, final number of nodes in the main ramification of 43 and number of primary and secondary ramifications of eight and 20, respectively.
For the emission of staminate and pistillate flowers the watermelon hybrids need an average accumulation of 10.5 and 46.7 °C days, respectively.They present a number of staminate and pistillate flowers of 52 and nine, respectively, and the ratio between flowers of 6.6:1.
Figure 5 second

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