Journal of Applied Botany and Food Quality 91, 281 - 286 (2018), DOI:10.5073/JABFQ.2018.091.036 1Federal University of São Francisco Valley, Center of Agrarian Sciences, Agronomic Engineering Course, Petrolina, Pernambuco, Brazil 2Produtiva consulting, Juazeiro, Bahia, Brazil A new approach to induce mango shoot maturation in Brazilian semi-arid environment Ítalo Herbert Lucena Cavalcante1*, Guilherme Neves Ferreira dos Santos1, Marcelle Almeida da Silva1, Rogério dos Santos Martins2, Augusto Miguel Nascimento Lima1, Pedro Igor Rodrigues Modesto1, Adilson Monteiro Alcobia1, Tullyus Rubens de Souza Silva1, Renata Araújo e Amariz1, Márkilla Zunete Beckmann-Cavalcante1 (Submitted: May 15, 2018; Accepted: July 26, 2018) * Corresponding author Summary The shoot maturation phase is important for growing mangoes be- cause it precedes the floral induction, when plants are under stress caused by high temperatures and low water availability. Abiotic stress could be alleviated by using plant biostimulant which alters the phytohormone and carbohydrates biosynthesis. Thus, an experi- ment was conducted to evaluate the use a plant biostimulant con- taining Ascophyllum nodosum to induce shoot maturation of mango cv. Palmer grown in semi-arid environment. The experimental design consisted of randomized blocks with four treatments, ten replications and five plants per parcel. Treatments consisted of: T1) biostimulant foliar spray + K fertilizer; T2) foliar spray with bio- stimulant alternating with K fertilizer; T3) individual foliar sprays with magnesium sulfate, potassium sulfate, sulfur and calcium ferti- lizers, potassium fertilizer and Ethrel®; and T4) Control treatment. The total soluble carbohydrates in leaves, buds and shoots, N, K and S leaf concentrations and fruit production were recorded. The carbo- hydrate concentrations, nitrogen, sulphur and potassium leaf concen- trations and fruit production of mango depend on shoot maturation strategy. Shoot maturation strategy using biostimulant containing Ascophyllum nodosum alternating with K fertilizer from 30 days after PBZ could be recommended for the production of mango cv. Palmer. Key words: Mangifera indica L., biostimulant, fruit production, car- bohydrate, algae extract. Introduction Mango (Mangifera indica) is a very important fruit crop for Brazil, which is the seventh most producing country and one of the largest mango exporter countries (Fao, 2017). In Brazil, mango is especially grown in São Francisco Valley, where more than 90% of Brazilian exported mango is produced (Alicew eb, 2017). Mango flowering has been demonstrated in field and in the scien- tific literature to be a complex event dependent of many factors con- cerning to climate conditions detaching that temperature is the most influential climatic factor (La x m a n et al., 2016), nutritional status (cava lca n t e et al., 2016; Ca r n ei ro et al., 2017), pruning (Asr ey et al., 2013), hormone balance (Ra m í r e z et al., 2014), carbohydrate concentration (Pr asa d et al., 2014; Ku m a r et al., 2014) and shoot maturation of the last vegetative flush, which has been measured as age of the last flush of vegetative stems, and it appears to be the pri- mary factor regulating floral induction in warm climates (Ra m í r e z et al., 2010). Mango shoot suitable for flowering induction was studied by Dav en p ort et al. (2006) who concluded that terminal stems (ter- minal intercalary units) must have attained a dark green color and achieved a minimum age of 4 months since the previous limp, red- leaf stage in easily induced cultivars and 5 months for the more re- calcitrant cultivars to obtain a reproductive shoot response in the low-latitude tropics; and Ra m í r e z et al. (2010) that stem age was the key factor correlated with flowering in the tropical conditions. In addition, it is necessary to stablish the physiological characteristics of a mango shoot suitable for flowering, which is defined as a ‘mature shoot’. Shoot maturation does not occur uniformly throughout the tree ś canopy and it is affected by shoot age, climate conditions and orchard management (non-published data), that could present crucial importance, especially for mango trees grown under adverse climate as occurs in São Francisco Valley. In this region mango has been grown under very high temperature and low air humidity averages, reaching 36.8 °C and 25.6% especially from September to December months (La bm et, 2016). This is a critical phase because it coincides with the pre-flowering-induction stage of those mango trees planned to produce fruits in April-May of the next year. In addition, during pre-flowering-induction phase mango is irrigated with lower water amounts, which is necessary to stimulate ethylene production and improve mango flowering (Ra m í r e z and Dav en p ort, 2016). Under adverse climate conditions, the use of biostimulants could be an option to improve shoot maturation, especially those containing algae extracts such as Ascophyllum nodosum, that promotes bene- fic effects on plant physiology but the more substantial improve- ments are associated with improving tolerance toward abiotic stress- es, including drought stress (Spann and Little, 2011), ion toxicity (Mancuso et al., 2006) and high temperature (Zhang and Ervin, 2008). Indeed, according to Wally et al. (2013) A. nodosum leaf sprays enhanced total concentration of cytokinins, abscisic acid (ABA) and ABA catabolite levels, whereas auxin levels reduction. The plant nutritional status also affects mango flowering (Gen ú and Pi n to, 2002), then the fertilizing management, especially for potas- sium, sulphur and nitrogen is crucial during the phase that precedes flowering induction, i.e., the shoot maturation. The key effect of po- tassium in plants is related to photosynthesis, plant respiration and solute translocations (Ma rsch n er, 2012); and sulphur is used on Yang cycle for ethylene biosynthesis (Pe ssa r a k li, 2014). On the other hand, at the time of flowering induction nitrogen concentrations should be in the lower average limit of adequate supply in order to avoid new vegetative flushes instead of reproductive phase (Dav en- p ort et al., 2003). Hence, the present study aimed to use a plant biostimulant containing Ascophyllum nodosum extract to induce shoot maturation of mango cv. Palmer grown in Brazilian semi-arid environment. Material and methods Plant material and growth conditions ‘Palmer’ mango (Mangifera indica L.) plants with uniform size and vigor, that were four years old thus in the first production cycle, were used in this study. The study was conducted from 2016 to 2017 in two experimental orchards located in Sebastião da manga farm in Casa Nova County 282 Í.H.L. Cavalcante, G.N.F. dos Santos, M.A. da Silva, R.S. Martins, A.M.N. Lima, P.I.R. Modesto, A.M. Alcobia, T.R.S. Silva, R. Araújo e Amariz, M.Z. Beckmann-Cavalcante (09°11’ S and 41º59’ W; at an altitude of 400.3 m above sea level), Bahia State, Brazil. The climate of this region is classified as Bswh (Köeppen), which corresponds to a semi-arid region. The average air temperature and air humidity ranged from 20.7 ºC to 35.4 ºC and from 61.4% and 88.7%, respectively, with accumulated precipitation of 194.8 mm. The plants, spaced with 5.0 m between the rows and 2.3 m between the plants, were daily drip-irrigated with one emitter at each 0.5 m, for a flow of 2.5 L h-1 each. All management practices such as prun- ing, control of weeds, pests and diseases, plant growth regulators for gibberellin inhibition (Cultar®) and break dormancy (calcium ni- trate) were performed following the instructions of Gen ú and Pi n to (2002). The nutrient management was performed through a fertirri- gation system, according to plant demand (Gen ú and Pi n to, 2002). Treatments and experimental design The experimental design consisted of randomized blocks with four treatments, ten replications and five plants in each parcel, reaching 50 plants per treatment. Treatments consisted of four strategies for shoot maturation of mango, as follows: T1) biostimulant foliar spray (2.5 ml L) + K fertilizer (2.5 mL L, 30% K2O); T2) foliar spray with biostimulant (2.5 ml L) alternating with K fertilizer (2.5 mL L, 30% K2O); T3) individual foliar sprays [magnesium sulfate (20 g L, 14% S and 10% Mg), potassium sulfate (25 g L, 17% S, 48% of K2O and 1.2% Mg), sulfur and calcium fertilizers (8 g L, 50% S and 5% Ca), potassium fertilizer (25 mL L, 55% K2O), and Ethrel® (3mL L)]; and T4) Control treatment. The biostimulant used contains N (1.3%), K2O (1.0%), Ca (3.0%), Mg (3.0%), S (3.56%), Mo (0.5%), organic carbon (2.69%), Ascophyllum nodosum extract (1.5%), amino acids (5.0%) and fulvic acids (2.0%). The treatments were applied according to the number of the days after the gibberellin inhibitor was applied, paclobutrazol (PBZ) ([(2RS, 3RS)-1-(4-clorofenil)-4,4-dimetil-2-(1H-1,2,4-triazol-1-il) pentan-3-ol]), in a ten days interval, beginning at 30 days after PBZ (T2) and 60 days after PBZ (T1 and T3), based on the traditional shoot maturation sprays (T3) used commercially. Data gathered and statistical analysis According to recommendations of Si lva (2009) leaf samples were collected in shoots from the middle part of the canopy to perform the potassium, sulphur [K and S at the beginning, middle and end of shoot maturation (flower induction)] and nitrogen (at the end of shoot maturation, which coincides with flowering induction) leaf concen- trations. Leaves were chemically analyzed after they were washed and rinsed with distilled water and dried at 65 oC until reach constant weight following methodology described by Si lva (2009). The K concentrations were determined by flame photometry, the N concen- trations by Kjeldahl method and the S contents were measured by turbidometry. The total soluble carbohydrates (TSC) concentrations were quanti- fied in leaves, buds and shoots from the beginning of shoot matura- tion until flowering induction, reaching five evaluation dates, follow- ing the methodology described by Du bois et al. (1956). At harvest the number of fruits per plant, fruit production and fruit yield (t ha-1) was calculated. Only commercial fruits were manu- ally harvested in a single day when they reached the physiologi- cal maturity which was characterized through pulp color (yellow cream), following the fruit selection parameter recommended by the br a z i li a n p rogr a m For hort icu lt u r e moder n i z at ion (2004) for commercial farms. Statistical analyses included analysis of variance (ANOVA) using combined data from the two experimental areas. All calculations were performed using the Assistat 7.7 software, and terms were considered significant at p < 0.01. Results and discussion All variables studied were affected by shoot maturation strategies, including those variables evaluated with time elapsing. Total soluble carbohydrates depended on shoot maturation strategy independently of the plant part (shoot, leaf or bud) (Fig. 2). As can be seen in Fig. 2A, leaf carbohydrate concentrations of all treatments increased from the first to the second evaluation date but only T4 presented a peak at the third date. A similar data distribution pre- sented in Fig. 2 was also recorded by Ur ba n et al. (2006) in study about season effects on leaf nitrogen partitioning and photosynthetic water use efficiency in mango. Indeed, from the third to the forth date It was registered a huge decrease in this variable especially for T4 (346%), T1 (250%) and T3 (154%), followed by stabilization at the end of shoot maturation (flower induction), when T2 was statistically higher than other treat- ments. The higher leaf carbohydrate concentration of T2 at the end of shoot maturation stage (flower induction) could be explained by the positive effects of Ascophyllum nodosum extract applied. Ac- cording to Wa lly et al. (2013) such products contain growth regula- tors (auxins, cytokinins and gibberellins), betain, amino acids and low concentrations of inorganic elements that influence cell growth and division cycle, expansion, nutrition and maturity. On the other hand, Kh a n et al. (2009) explained that the mechanism(s) of actions of seaweed extract-elicited physiological responses are largely un- known and the algae extract effect on plants depends on plant spe- cies, soil, climate and crop management at all. The leaf carbohydrate concentration of Fig. 2A are close to that re- corded by Ur ba n et al. (2006) and higher than average value quoted by Pr asa d et al. (2014) for the same phenological phase of the pre- sent study. In shoots (stem of the last vegetative flush) total soluble carbohy- drates concentration also presented the same tendency for T2 and T4, i.e., average enhancement until the third evaluation and stabilization for the last evaluation date (Fig. 2B). Carbohydrate concentrations in shoots were lower than those registered in leaves, independently of the evaluation date, but at the end of shoot maturation phase T2 also presented significantly higher carbohydrate concentration that Fig. 1: Time scale of the main events during the experiments. Flowering induction T1 spray T1 spray T1 spray T1 spray WBR begins T3 spray T3 spray T3 spray T3 spray T2 spray T2 spray T2 spray T2 spray T2 spray T2 spray WBR ends Fruit harvest 30 40 50 60 70 80 90 240 Days after PBZ application WBR begins = Water blade reduction begins; WBR ends = Water blade reduction ends A new approach to induce mango shoot maturation 283 is a positive scenario since source-to-sink transport of sugar is one of the major determinants of plant growth and relies on the efficient and controlled distribution of sucrose (and some other sugars such as raffinose and polyols) across plant organs through the phloem. How- ever, sugar transport through the phloem can be affected by many environmental factors that alter source sink relationships (Lemoi n e et al., 2013). It is important to note the lower carbohydrate concentrations de- crease recorded for T2 in both leaves and shoots from the middle to the end of shoot maturation phase, showing that plants of this treat- ment at the flowering induction (end of the shoot maturation) pre- sented higher soluble carbohydrate concentrations. The other hand, soluble carbohydrates in buds (Fig. 2C) presented a different data distribution as a function of the dates during shoot maturation, except for T2. It is relevant to point the extremely higher average recorded to the non-treated plants at the end of shoot matura- tion, because these plants presented very poor or no flowers, show- ing that for mango high carbohydrate concentration in buds is not a key for good flowering and fruit production. Whether compared to Pr asa d et al. (2014) data it is verified that average value recoded for T4 (control treatment) is extremely higher. Leaf concentrations for potassium, sulphur and nitrogen depended on shoot maturation strategy (Fig. 3). Independently of the treatment, K leaf concentrations enhanced with time elapsing until reach a peak at the end of shoot maturation when T2 and T3 were above the other treatments. During shoot maturation phase the key effect of potassi- um in plants is related to photosynthesis, plant respiration and solute translocations (Ma rsch n er, 2012). Whether compared with Ma lavolta et al. (1997) adequate range of supply (4.0-6.0 g kg-1), it verifies that at the end of shoot matu- ration (flower induction) plants of all treatments presented higher averages. The other way, for the adequate range of supply reported by Pi m plask er and Bh a rgava (2003), i.e. 1.02-2.01% (or 10.2- 20.1 g kg-1), plants of all treatments had adequate K leaf concentra- tions. Comparatively, the average foliar potassium values presented in Fig. 3A were higher than those recorded by Cava lca n t e et al. (2016) in study about K fertilizing of ‘Palmer’ mango under semi- arid environment. Sulphur leaf concentrations of T1, T2 and T4 were similar among them and presented a soft variation during shoot maturation phase (Fig. 3B), but, T3 promoted a S leaf concentration peak at the middle of shoot maturation, followed by a huge decay of 300% until the end of this phase. This data distribution could be caused by the fo- liar spray with sulphates performed in T3 followed by Ethrel® leaf Fig. 2: Total soluble carbohydrates concentrations in leaves (A), shoots (B) and buds (C) of mango cv. Palmer as a function of branch maturation strategy in five evaluation dates. Points with the same letters do not differ in among themselves by Tukey’s test at 1% probability in each evaluation date. T1) biostimulant foliar spray + K fertilizer; T2) foliar spray with biostimulant alternating with K fertilizer; T3) individual foliar sprays (magnesium sulfate, potassium sulfate, sulfur and calcium fertilizers, potassium fertilizer, and Ethrel®; and T4) Control treatment. FM = fresh mass. 30 50 70 90 110 T1 T2 T3 T4 01 11 18 11 28 11 07 12 16 12 a b a a a b b b a a b C ar bo hy dr at es in s ho ot s (m g g- 1 o f F M ) Evaluation dates ! Evaluation dates ! Evaluation dates 50 100 150 200 250 300 T1 T2 T3 T4 01 11 18 11 28 11 07 12 16 12 a a a a b b a a a C ar bo hy dr at es in le av es (m g g- 1 o f F M ) b 0 50 100 150 200 250 T1 T2 T3 T4 C ar bo hy dr at es in b ud s (m g g -1 of F M ) a a a a a b a b b a 01 11 18 11 28 11 07 12 16 12 A B C 30 50 70 90 110 T1 T2 T3 T4 01 11 18 11 28 11 07 12 16 12 a b a a a b b b a a b C ar bo hy dr at es in s ho ot s (m g g- 1 o f F M ) Evaluation dates ! Evaluation dates ! Evaluation dates 50 100 150 200 250 300 T1 T2 T3 T4 01 11 18 11 28 11 07 12 16 12 a a a a b b a a a C ar bo hy dr at es in le av es (m g g- 1 o f F M ) b 0 50 100 150 200 250 T1 T2 T3 T4 C ar bo hy dr at es in b ud s (m g g -1 of F M ) a a a a a b a b b a 01 11 18 11 28 11 07 12 16 12 A B C 284 Í.H.L. Cavalcante, G.N.F. dos Santos, M.A. da Silva, R.S. Martins, A.M.N. Lima, P.I.R. Modesto, A.M. Alcobia, T.R.S. Silva, R. Araújo e Amariz, M.Z. Beckmann-Cavalcante spray, an ethylene precursor, in which production cycle uses S for Yang cycle (Pe ssa r a k li, 2014). Independently of the shoot matura- tion strategy studied, all treatments were within the stated adequate range of supply 1.1-1.7 g kg-1 properly described by Pi m plask er and Bh a rgava (2003). As can be seen in Fig. 4C, N leaf concentrations at the end of shoot maturation (flower induction) also depended on shoot maturation strategies, with statistically high average recorded for T4 (control treatment). According to Pi m plask er and Bh a rgava (2003) the N leaf concentration considered as adequate for mangoes range from 8.9 to 19.3 g kg-1, but there is controversy because according to Dav en p ort et al. (2003) the leaf N levels for mango should be at 11 to 14 g kg-1 at the time of flowering induction in order to avoid new vegetative flushes instead of reproductive phase, i.e., N leaf concentration should be in maximum 14 g kg-1. On the other hand, in the present study T1, T2 and T3 presented commercial fruit yields with leaf N concentrations of 14.4, 14.7 and 15.1 g kg-1 respectively, while T4 presented no fruit production with N leaf concentration of 18.1 g kg-1 showing that adequate maximum N leaf concentration at flowering induction depends on mango cultivar and the production system used. Fruit production variables depended on treatments studied (Fig. 4), and that plants of control treatment presented a very poor fruit production, including lots of parcels presented no fruit production making not possible to perform statistical analysis for this treatment. Fruit production variables presented the same data tendency, i.e., T2 promoted the higher number of fruits per plant, fruit production and fruit yield (Fig. 4). For number of fruits per plant T2 presented an average almost 46% higher than T3, the second higher average, and it reached 94.8 commercial fruits per plants. Cava lca n t e et al. (2016) recorded a maximum number of commercial fruits per plant of 294, but in eleven years old plants, that’s different from the current study which used four years old plants, in the first production cycle. Fruit production (kg per plant) ranged from 28.14 kg plant (T1) to 38.62 kg plant, which is lower than other scientific results in the literature such as Cava lca n t e et al. (2016), Wa h da n et al. (2011) in Egypt, 82.71-88.86 kg plant reported by Ye sh i t ela et al. (2005) in South Africa, Qu i ja da et al. (2009) in Venezuela and Sa r a n and Ku m a r (2011) in India. On the other hand, except for Cava lca n t e et al. (2016), all authors quote the total fruit production per plant and not a commercial fruit production, in orchards with wide spaces be- tween plants were, naturally, the plants are higher and produce more fruits, so the crucial comparison must refer to fruit yield. Following the same tendency of the number of fruits per plant and fruit production (kg plant), the commercial fruit yield (t ha) was significantly higher to T2 which promoted an average of 33.6 t ha (Fig. 4C), thus 20% and 27% higher than those quoted to T3 (26.89 t ha) and T1 (24.48 t ha) respectively. The fruit yield promoted by T2 is compatible to average value recorded by Ba r bosa et al. (2016) (36.6 t ha) for ‘Palmer’ and higher than 27 t ha of Cava lca n t e et al. (2016) for ‘Palmer’, 10.5 ton ha-1 of Plegu e z u elo et al. (2012) in Spain as well as higher than in the main worldwide producer coun- tries such as Brazil (16.1 t ha), China (8.2 t ha), India (7.3 t ha) and Mexico (8.9 t ha) (Fao, 2017). 0 1 2 3 4 5 6 7 T1 T2 T3 T4 01 11 28 11 19 12 S le af c on ce nt ra tio n (g k g- 1 ) 14.14 b 14.7 b 15.07 b 18.11 a 0 2 4 6 8 10 12 14 16 18 20 T1 T2 T3 T4 N le af c on ce nt ra tio n (g k g- 1 ) b Branchmaturation strategy C 4 6 8 10 12 14 16 T1 T2 T3 T4 01 11 28 11 19 12 K le af c on ce nt ra tio n (g k g- 1 ) a a a a a a b b Evaluation dates BA Evaluation dates Fig. 3: Leaf concentrations of potassium (A), sulphur (B) at the beginning, middle and end of shoot maturation; and nitrogen (C) at the end of shoot matura- tion of mango cv. Palmer as a function of shoot maturation strategy. Points or bars with the same letters do not differ in among themselves by Tukey’s test at 1% probability in each evaluation date. T1) biostimulant foliar spray + K fertilizer; T2) foliar spray with biostimulant alternating with K fertilizer; T3) individual foliar sprays (magnesium sulfate, potassium sulfate, sulfur and calcium fertilizers, potassium fertilizer, and Ethrel®; and T4) Control treatment. A new approach to induce mango shoot maturation 285 The superiority recorded for the treatment with algae extract leaf spray applied individually could also be explained by the anti-stress characteristics of this product since during maturation phase the temperatures were high (36.8 ºC) the air humidity was low (25.6%) and mango plants were exposed to water blade reduction. This way, La n e et al. (2006) argue that Ascophyllum nodosum contain the polysaccharides laminaran, fucoidan, and alginate and laminarin has been shown to stimulate natural defense responses in plants and is involved in the induction of genes encoding various pathogenesis- related proteins with antimicrobial properties. In a general form, positive effects of Ascophyllum nodosum extracts were previously reported by Mor a le s-Paya n (2013) during seed- ling formation phase and Moh a m ed and El-Seh r aw y (2013), who recorded better plant nutrition and fruit retention of mango. Conclusion Thus, the results of this study indicate that: i) carbohydrate con- centrations, nitrogen, sulphur and potassium leaf concentrations and fruit production of mango ‘Palmer’ depend on shoot matura- tion strategy; ii) under the soil, climate and plant conditions of this study, shoot maturation strategy using foliar spray with biostimulant containing Ascophyllum nodosum alternating with K fertilizer from 30 days after PBZ use could be recommended for the production of mango ‘Palmer’ in the semi-arid environment; iii) the very poor fruit production of the control plants is a clear indication of the im- portance to induce shoot maturation for growing mangoes for com- mercial purposes in the semi-arid environment. On the other hand future research is demanded to study effects of shoot maturation in different mango cultivars and/or mango grown in warm climates or different seasons. Acknowledgements The authors gratefully thank to Global Crops® for granting the sup- port necessary to carry out the research, and to Sebastião da Manga farm (Casa Nova County, Bahia state, Brazil) for structural support necessary for execution of the experiments. References a l ic ew e b. Sistema de Análise das Informações de Comércio Exterior, 2016. Retrieved 20th October 2017, from http://aliceweb.desenvolvim- ento.gov.br asr ey, r., pat e l, v., ba r m a n, k., pa l, r., 2013: Pruning affects fruit yield and postharvest quality in mango (Mangifera indica L.) cv. Amra- pali. Fruits. 68, 367-380. DOI: 10.1051/fruits/2013082 ba r bosa, l.F. s., cava l ca n t e, i.h.l., li m a, a.m.n., 2016: Desordem fisiológica e produtividade de mangueira cv. Palmer associada à nutrição de boro. Rev. Bras. Frutic. 38, 1-10. 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DOI:10.2135/cropsci2007.05.0262 Address of the corresponding author: Federal University of São Francisco Valley, Center of Agrarian Sciences, Agronomic Engineering, Rodovia BR 407 - KM 119 - Lote 543 PSNC, s/nº - C1, 56300-990, Petrolina, Pernambuco, Brazil. E-mail: italo.cavalcante@univasf.edu.br © The Author(s) 2018. This is an Open Access article distributed under the terms of the Creative Commons Attribution Share-Alike License (http://creative- commons.org/licenses/by-sa/4.0/).