This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and

Transcription

1 This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier s archiving and manuscript policies are encouraged to visit:

2 Scientia Horticulturae 129 (2011) Contents lists available at ScienceDirect Scientia Horticulturae journal homepage: Horticultural performance of Folha Murcha sweet orange onto twelve rootstocks Tatiana Cantuarias-Avilés a, Francisco de Assis Alves Mourão Filho a,, Eduardo Sanches Stuchi b, Simone Rodrigues da Silva a, Erick Espinoza-Nuñez a a Universidade de São Paulo, Escola Superior de Agricultura Luiz de Queiroz, Piracicaba, SP, Brazil b Embrapa Mandioca e Fruticultura, Estação Experimental de Citricultura de Bebedouro, Bebedouro, SP, Brazil article info abstract Article history: Received 5 December 2010 Received in revised form 18 March 2011 Accepted 22 March 2011 Keywords: Canopy volume Yield efficiency Drought tolerance Citrus variegated chlorosis Citrus sinensis Leaf color Despite its outstanding position, the Brazilian citriculture is established on a very limited pool of varieties that limits its expansion and restricts the fruit availability throughout the year. This situation determines the urgent necessity of developing alternative scion and rootstock cultivars, with good performance under local conditions. Folha Murcha sweet orange (Citrus sinensis (L.) Osbeck) is a late-harvest cultivar, suitable both for the juice processing industry and the fresh fruit market, being described as tolerant to citrus canker (Xanthomonas citri subsp. citri Schaad et al.), and less affected by citrus variegated chlorosis (Xylella fastidiosa Wells et al.). A study was conducted in Bebedouro, São Paulo State, Brazil, to evaluate the horticultural performance of Folha Murcha sweet orange budded onto 12 rootstocks: the citrandarin Changsha mandarin (Citrus reticulata Blanco) Poncirus trifoliata English Small ; the hybrid Rangpur lime (Citrus limonia Osbeck) Swingle citrumelo (P. trifoliata (L.) Raf. Citrus paradisi Macfad.); the trifoliates (P. trifoliata (L.) Raf.) Rubidoux, FCAV, and Flying Dragon (P. trifoliata var. monstrosa); the Sun Chu Sha Kat mandarin (C. reticulata Blanco); the Sunki mandarin (Citrus sunki (Hayata) Hort. ex. Tanaka); the Rangpur limes (C. limonia Osbeck) Cravo Limeira and Cravo FCAV ; Carrizo citrange (C. sinensis P. trifoliata), Swingle citrumelo (P. trifoliata C. paradisi), and Orlando tangelo (C. paradisi Citrus tangerina cv. Dancy ). The experimental grove was planted in 2001, using a 7 m 4 m spacing, in a randomized block design, with five replications and two plants per plot. No supplementary irrigation was applied. Fruit yield, canopy volume, tree tolerance to drought and to citrus variegated chlorosis, and fruit quality were assessed for each rootstock. Trees grafted onto the Flying Dragon trifoliate were smaller in size, but had largest yield efficiency when compared to those grafted onto other rootstocks. Lower alternate bearing index was observed on trees budded onto Cravo FCAV Rangpur lime. Both Rangpur lime rootstocks and the Sunki mandarin induced higher tree tolerance to drought. The Flying Dragon trifoliate induced better fruit quality and higher tolerance to citrus variegated chlorosis (CVC) to Folha Murcha trees. A cluster multivariate analysis identified three groups of rootstocks with similar effects on Folha Murcha tree performance. Among the 12 evaluated rootstocks, the Flying Dragon trifoliate has a unique effect on plant growth, tolerance to drought and CVC, fruit yield and fruit quality of Folha Murcha trees, and may be better suited for high-density plantings Elsevier B.V. All rights reserved. 1. Introduction Diversification of current rootstock and scion citrus cultivars is very important for Brazilian citriculture in order to reduce the high risks associated with the outbreaks of new and more severe diseases and pests spreading over a narrow genetic pool (Bové and Ayres, 2007). Brazil is the world s largest sweet orange juice producer, exporting more than 1,300,000 t per year. The State of São Paulo is the largest growing region, with 599,730 ha, mainly cultivated with Pêra, Natal, Valencia and Hamlin scions budded Corresponding author. Tel.: ; fax: address: francisco.mourao@usp.br (F.A.A. Mourão Filho). onto Rangpur lime (FNP, 2010). Among the sweet orange cultivars that have been recently selected to extend fruit supply to the local juice industry, the Folha Murcha scion was obtained from a natural local mutation, and it is suitable for both the industry and the fresh fruit markets (Hodgson, 1967; Stuchi et al., 2000a). Fruits of Folha Murcha sweet orange have high juice and sugar contents, with excellent juice color and longer fruit retention on the tree. Folha Murcha trees are also very resistant to drought and tolerant to the citrus canker (Xanthomonas citri subsp. citri Schaad et al.) (Leite and Mohan, 1988), and less affected by CVC (Xylella fastidiosa Wells et al.) (Molina et al., 2010). This work reports the response of Folha Murcha trees budded onto 12 rootstocks in the Northern region of São Paulo State, with emphasis on rootstock influence over canopy volume, fruit /$ see front matter 2011 Elsevier B.V. All rights reserved. doi: /j.scienta

3 260 T. Cantuarias-Avilés et al. / Scientia Horticulturae 129 (2011) yield and fruit quality, and plant tolerance to drought and to CVC. A multivariate clustering analysis technique was utilized to identify aggregates of rootstocks that induced similar characteristics to Folha Murcha trees, considering 14 evaluated variables that were significantly affected by the rootstocks. 2. Material and methods 2.1. Field trial and plant material The experimental grove was planted in February 2001 at the Estação Experimental de Citricultura de Bebedouro, located in the Northern region of São Paulo State ( S latitude, W longitude, 680 m altitude), in a 7 m 4 m spacing (357 plants ha 1 ), on a total area of 4032 m 2. The climate is Köeppen s Cwa, with a mean temperature of 23.5 C and an annual rainfall of 1522 mm. The soil is classified as Haplustox (38% clay) (EMBRAPA, 1999). Folha Murcha sweet orange was budded onto each one of the following 12 rootstocks (treatments): Carrizo citrange; the hybrid Cravo Rangpur lime Swingle citrumelo; the citrandarin Changsha English Small ; the Sun Chu Sha Kat mandarin; the Sunki mandarin; the trifoliates Rubidoux, FCAV, and Flying Dragon ; the Cravo Limeira and Cravo FCAV Rangpur limes; Swingle citrumelo, and Orlando tangelo. No supplemental irrigation was applied. Trees were not pruned and standard cultural practices for citrus were applied (Mattos Júnior et al., 2005) Plant yield, canopy volume, yield efficiency and alternate bearing index Yield per plot was recorded for each commercial harvest. Cumulative yield was calculated from 2004 to 2008 (years 3 7 after planting), while the percentage of cumulative yield at the second commercial harvest (2005) was estimated to assess the rootstock effect on early-bearing. Canopy volume (V) was determined from individual measurements of tree height (H) and width in parallel (D l ) and perpendicular (D r ) directions to the tree row in May ( ), assuming that the tree shape was one half prolate spheroid, using the formula: V =(/6) H D l D r (Zekri, 2000). Projected tree spacing and fruit yield for high density planting of Folha Murcha sweet orange budded onto Flying Dragon trifoliate were calculated from tree diameter and yield measured in 2008 (7 years after planting). The distance between rows was computed by adding 2.5 m to the mean plant diameter measured in 2008, while plant spacing along the row was determined by multiplying the mean plant diameter in 2008 by 0.85 m, assuming a 15% canopy overlapping along the row (De Negri and Blasco, 1991). Yield efficiency (YE) was computed from the relationship between fruit yield (kg plot 1 ) and canopy volume (m 3 plot 1 ) ( ). The relationship between YE and V was analyzed by a regression model. The alternate bearing index (ABI) was calculated from 2004 to 2008, using the following expression: ABI = 1/(n 1) { a 2 a 1 /(a 2 + a 1 )+ a 3 a 2 /(a 3 +a 2 )+...+ a n a n 1 /(a n +a n 1 )}, where n = number of years and a 1, a 2,..., a n 1, a n = yield of the corresponding years (Stenzel et al., 2003) Plant tolerance to drought and to citrus variegated chlorosis Drought tolerance was evaluated from 2006 to 2008 during the winter dry period (August), using two approaches: (i) visual assessment of canopy water stress of each tree, based on a three-score rating scale (scores 1 3 for low, medium and high tolerance to water stress, respectively, for decreasing canopy wilting and defoliation intensities) (Stuchi et al., 2000b); and (ii) leaf color (Deidda et al., 1996), measured with a Minolta CR-300 colorimeter and estimated through the variables L* (luminosity), C* (chromaticity) and h (hue or color angle), on samples of 20 leaves per treatment. L* ranges from black (0) to white (100). C* values closer to zero represent grey colors, while values closer to 60 express vivid colors. Hue (h ) angles closer to 180 represent greener colors, while values closer to 90 indicate yellowish color. Green leaf color was described by low L, low C and high h values. CVC was evaluated by visual observation of symptoms in the canopy, using a 0 3 score rating scale (0, asymptomatic tree; 1, tree with one symptomatic branch; 2, tree with more than one symptomatic branch and up to 50% of symptomatic canopy; 3, tree with more than two symptomatic branches and fruits affected by the disease) (Cao et al., 2010; Denecke, 2006). The CVC percentage incidence (PI) was calculated from the number of symptomatic trees (rated with CVC scores > 0) among the total plants grafted onto each rootstock. A disease severity index (SI) was computed from the expression: SI = (n 0 0)+(n 1 1) + (n 2 2)+(n 3 3), where n 0, n 1, n 2 and n 3 are the number of trees evaluated with scores 0 3, respectively (Denecke, 2006) Fruit quality measurements Fruit quality was assessed from 2006 to 2008, on samples of five fruits collected from each plot in the commercial harvest. The following variables were measured: (i) fruit size, assessed for each sample by measuring the fresh weight and equatorial diameter; (ii) juice content (JC, %), from the relationship between the weight of the extracted juice and the fruit sample weight; (iii) total soluble solids content (TSS), expressed in Brix, by direct reading in a temperature-compensated digital refractometer; (iv) titratable acidity (TA), expressed as percentage of citric acid, by titration of 25 ml of juice with 0.31 N NaOH, (v) maturation index (MI), calculated by the ratio of TSS:TA, and (vi) the technological index (TI), expressed as kg of TSS per box of 40.8 kg (kg SST box 1 ), and calculated by the formula: TI = [JC SST 40.8] 10,000 1 (Cavalcante et al., 2009) Experimental design and data analysis The experiment was conducted following a randomized complete block design, with five replications and two plants per replication, with a total of 72 plots (144 trees). Data were analyzed by the Fisher s and Friedman s tests, for parametric and nonparametric analyses, respectively. The nonparametric approach was used for ordinal variables (scores). Original data of cumulative yield, canopy volume, yield efficiency [ŷ = log 10 (y)] and technological index [(ŷ = y 0.2 )] were transformed using the Box Cox method to follow a normal distribution. Comparisons among means were performed by the Tukey s test (P < 0.05 significance level). Data of 14 variables that were influenced by the rootstocks (cumulative yield, percentage of total cumulative yield assessed in the second commercial harvest, alternate bearing index, yield efficiency, canopy volume variation in the period, drought tolerance mean score, fruit weight, fruit diameter and height, JC, TSS, TA, MI and TI) were submitted to a multivariate cluster analysis, in order to classify rootstocks in groups of closer similarity, according to their general horticultural performance. Hierarchical cluster analysis was applied on standardized means of the 14 variables by using the single linkage method, and is shown on a dendrogram (Manly, 2005). 3. Results 3.1. Plant yield and canopy volume Cumulative yield ( ) of non-irrigated Folha Murcha sweet orange was significantly larger when budded onto Rubidoux trifoliate, followed by Cravo FCAV Rangpur lime and Swingle

4 T. Cantuarias-Avilés et al. / Scientia Horticulturae 129 (2011) Table 1 Cumulative yield after 7 years planting ( ), percentage of cumulative yield in the second commercial harvest (2005) and alternate bearing index (ABI) for nonirrigated Folha Murcha sweet orange trees budded onto 12 rootstocks. Bebedouro, SP, Brazil. Rootstock Cumulative yield after 7 years planting ( ) (t ha 1 ) * Percentage of cumulative yield in the second commercial harvest (2005) ** ABI ( ) Rubidoux trifoliate a 9.33 cd 0.43 ab Cravo FCAV Rangpur lime ab ab 0.23 b Swingle citrumelo ab abcd 0.33 ab Sun Chu Sha Kat mandarin abc bcd 0.48 a Sunki mandarin abc abcd 0.28 ab Changsha English Small hybrid abc cd 0.41 ab Cravo Swingle hybrid abc abcd 0.48 a Cravo Limeira Rangpur lime abc abc 0.30 ab Carrizo citrange abc abcd 0.45 ab FCAV trifoliate abc abcd 0.37 ab Orlando tangelo c 6.63 d 0.42 ab Flying Dragon trifoliate d a 0.27 ab CV (%) P-value < Means followed by different letters in columns are significantly different at the indicated P-value (Fisher s test) by Tukey s test (P < 0.05). * Original data were transformed (ŷ = log 10 y) to follow a normal distribution. ** Friedman s test at the indicated P-value. citrumelo. Trees grafted onto Carrizo citrange, FCAV trifoliate, the hybrids Cravo Swingle and Changsha English Small, and the Sun Chu Sha Kat and Sunki mandarins had similar yields to those of trees grafted onto Cravo Limeira Rangpur lime. Nonetheless, Folha Murcha trees had the lowest cumulative yields when budded onto Flying Dragon trifoliate, followed by those budded on Orlando tangelo (Table 1). No symptoms of scion rootstock incompatibility, such as low vigor, wilting, rootstock or scion overgrowth at the graft junction, were observed at any time during this study. The percentage of cumulative yield at the second commercial harvest (2005) was utilized to characterize the rootstock effect on the early bearing of Folha Murcha sweet orange (Table 1). The largest percentage of cumulative yield at the second harvest was recorded on trees budded onto the Flying Dragon trifoliate (34.52%), while the lowest percentage was observed on Orlando tangelo (6.63%). From 2004 to 2008, Folha Murcha sweet orange trees showed the highest alternate bearing index (ABI) when budded onto the Cravo Swingle hybrid and the Sun Chu Sha Kat mandarin. The lowest alternate bearing index values were recorded on trees grafted onto the Cravo FCAV Rangpur lime (Table 1). Between the 5th and the 7th year after planting ( ), the Folha Murcha trees budded onto Orlando tangelo had larger canopy volume values, followed by Sun Chu Sha Kat mandarin YE (kg/m 3 /plot) 10,0 9,0 8,0 7,0 6,0 5,0 4,0 3,0 2,0 1,0 0,0 'Flying Dragon' Trifoliata 'FCAV' 'Cravo FCAV' 'Cravo Limeira' 'Sunki' y = x R 2 = ** r 2 = ** 'Sun Chu Sha Kat' 'Orlando' 0,0 5,0 10,0 15,0 20,0 25,0 30,0 V (m 3 /plot) Fig. 1. Linear relationship between yield efficiency (YE) and canopy volume (V) of Folha Murcha sweet orange plots budded onto 12 rootstocks. Bebedouro, SP, Brazil, and Rubidoux trifoliate rootstocks (Table 2). The largest yield efficiency of Folha Murcha trees budded onto Flying Dragon trifoliate contrasted with the reduced canopy volume induced by this rootstock (Table 2). A highly significant linear relationship (P < ) between yield efficiency and canopy volume (Fig. 1) confirmed the superior performance of the Flying Dragon trifoliate as rootstock Table 2 Canopy volume, yield efficiency and drought tolerance of Folha Murcha sweet orange budded onto 12 rootstocks. Bebedouro, SP, Brazil, Rootstock Canopy volume (m 3 tree 1 ) * Yield efficiency * (kg m 3 ) Drought tolerance score ** Flying Dragon trifoliate 2.83 g 8.79 a 1.05 g FCAV trifoliate 8.09 fg 7.63 ab 1.26 efg Cravo Swingle hybrid def 6.86 ab 1.56 def Swingle citrumelo ef 6.36 abcd 1.63 de Changsha English Small hybrid bcde 5.77 abcd 1.69 de Carrizo citrange def 5.64 abcd 1.06 fg Cravo FCAV Rangpur lime bcde 5.32 bcd 2.97 a Rubidoux trifoliate abc 5.46 abcd 2.06 bcd Cravo Limeira Rangpur lime cdef 3.90 de 2.75 ab Sunki mandarin abcd 4.52 cde 2.35 abc Sun Chu Sha Kat mandarin ab 4.15 de 2.01 bcd Orlando tangelo a 2.83 e 1.55 ef CV (%) P-value < < < * Means followed by different letters in columns are significantly different at the indicated P-value (Fisher s test) by the Tukey s test (P < 0.05). Original data were transformed to follow a normal distribution [ŷ = log 10(y)]. ** Scores 1 3: low, medium and high canopy tolerance to drought, respectively. Friedman s test at the indicated P-value.

5 262 T. Cantuarias-Avilés et al. / Scientia Horticulturae 129 (2011) Table 3 Citrus variegated chlorosis (CVC) score, percentage incidence (PI) and severity index (SI) of Folha Murcha sweet orange trees budded onto 12 rootstocks. Bebedouro, SP, Brazil, Rootstock CVC score * PI ** (%) SI *** Sun Chu Sha Kat mandarin 2.70 a 100 a 4.80 a Rubidoux trifoliate 2.20 a 100 a 3.80 ab Orlando tangelo 1.80 ab 90 ab 3.60 ab Carrizo citrange 2.10 a 80 ab 3.60 ab Cravo FCAV Rangpur lime 1.90 ab 70 ab 3.20 ab FCAV trifoliate 1.70 ab 70 ab 2.80 ab Cravo Swingle hybrid 1.60 ab 70 ab 2.60 ab Cravo Limeira Rangpur lime 1.50 ab 60 ab 3.00 ab Sunki mandarin 1.30 ab 70 ab 2.60 ab Swingle citrumelo 1.30 ab 50 ab 2.00 ab Changsha English Small hybrid 1.10 ab 50 ab 2.20 ab Flying Dragon trifoliate 0.20 b 10 b 0.40 b CV (%) P-value Means followed by different letters in columns are significantly different at the indicated P-value (Friedman s test) by the Tukey s test (P < 0.05). * 0, Asymptomatic canopy; 3, severe canopy symptoms. ** % of plants with scores > 0. *** After Denecke (2006). for the Folha Murcha sweet orange, differing from the lowest productivity observed on trees budded onto the Orlando tangelo. For the Folha Murcha trees grafted onto Flying Dragon trifoliate, the projected tree spacing and yield for high density plantings were calculated from the mean canopy diameter (1.40 m) and yield (17.8 kg plant 1 ) recorded in 2008, 7 years after planting (De Negri and Blasco, 1991). From these data, the Folha Murcha / Flying Dragon combination might be planted at a 4 m 1m spacing (2500 plants ha 1 ), with a projected yield of 44.5 t ha 1 at the 7th year after planting, compared with the 7 m 4 m spacing (357 plants ha 1 ) utilized in this study, that yielded 6.34 t ha 1 after 7 years from planting, under non-irrigated conditions Plant tolerance to drought From 2006 to 2008, mean drought tolerance of Folha Murcha trees was the highest when grafted onto the Cravo FCAV and Cravo Limeira Rangpur limes, followed by plants grafted onto the Sunki mandarin. The Flying Dragon trifoliate rootstock induced the lowest drought resistance to Folha Murcha trees, followed by Carrizo citrange and FCAV trifoliate (Table 2). Leaf colorimetric variables L*, C* and h of Folha Murcha sweet orange, as measured in 2008 on the different rootstocks, were highly correlated with mean canopy drought tolerance scores assessed by visual evaluations from 2006 to Polynomial regression curves described a good fit between the three leaf colorimetric variables and the mean drought tolerance score, resulting in highly significant regression coefficients (Fig. 2) Plant tolerance to citrus variegated chlorosis In 2008, significant differences on the CVC score, percentage incidence and severity index were registered on Folha Murcha trees budded onto the different rootstocks (Table 3). Higher CVC score, percentage incidence and severity index values were recorded on trees grafted onto Sun Chu Sha Kat mandarin and Rubidoux trifoliate rootstocks. On the other hand, the lowest values for the three variables were observed onto the Flying Dragon trifoliate (Table 3). L* leaf (2008) C* leaf (2008) h o leaf (2008) y = 1.787x x R 2 = Drought tolerance mean score ( ) y = x x R 2 = Drought tolerance mean score ( ) y = x x R 2 = Drought tolerance mean score ( ) Fig. 2. Polynomial regression curves describing the relationship between leaf colorimetric variables L, C and h and the drought tolerance mean score on trees of Folha Murcha sweet orange budded onto 12 rootstocks. Bebedouro, SP, Brazil Fruit quality Fruit quality was evaluated on each commercial harvest from 2006 to 2008 (5 7th year after planting) (Table 4). Larger fruit weight was found on trees grafted onto the Cravo FCAV and Cravo Limeira Rangpur limes, contrasting with lighter fruits picked on trees budded onto the Orlando tangelo. Despite of the higher JC conferred by the Cravo Limeira Rangpur lime, this rootstock induced the lowest TSS, TA and TI to Folha Murcha sweet oranges (Table 4). On the other hand, the fruits picked onto Flying Dragon trifoliate had high TSS and TA, but low JC and TI. Yet, the FCAV trifoliate conferred the highest fruit quality to

6 T. Cantuarias-Avilés et al. / Scientia Horticulturae 129 (2011) Table 4 Fruit quality of Folha Murcha sweet orange as influenced by 12 rootstocks. Bebedouro, SP, Brazil, Rootstock Fruit weight (g) JC (%) TSS ( Brix) TA (%) MI TI * kg SST box 1 Carrizo citrange ab ab a 1.24 ab ab 2.50 b Cravo Swingle hybrid ab ab a 1.28 a ab 2.56 ab Sun Chu Sha Kat mandarin ab ab a 1.36 a 9.65 b 2.50 b Rubidoux trifoliate ab ab a 1.26 a ab 2.58 ab Changsha E.Small hybrid ab ab ab 1.14 ab a 2.48 b Cravo Limeira Rangpur lime a a b 0.99 b a 2.45 b Swingle citrumelo ab ab a 1.26 a ab 2.61 ab Orlando tangelo b ab ab 1.34 a ab 2.46 b FCAV trifoliate ab a a 1.28 a ab 2.75 a Flying Dragon trifoliate ab b a 1.27 a ab 2.47 b Sunki mandarin ab a ab 1.18 ab ab 2.48 b Cravo FCAV Rangpur lime a ab a 1.13 ab ab 2.48 b CV (%) P-value JC, juice content; TSS, total soluble solids; TA, titratable acidity; MI (Maturity Index), TSS/TA; TI (technological index) [JC TSS 40.8] 10, Means followed by different letters in columns significantly differ at the indicated P-value (Fisher s test) by the Tukey s test (P < 0.05). * Original data were transformed to follow a normal distribution [ŷ = y 0.2 ]. Folha Murcha sweet oranges, considering all the evaluated variables Rootstock effect on the overall tree performance The dendrogram obtained from the multivariate cluster analysis indicated three different aggregates of rootstocks with similar effects on the horticultural performance and fruit quality of Folha Murcha sweet orange (Fig. 3). The first cluster of rootstocks with similar effects were the Cravo Swingle hybrid and the Swingle citrumelo, both inducing very similar characteristics to the Folha Murcha scion, probably due to the genetic proximity between both rootstocks (Pompeu Júnior et al., 1997). A second cluster included the Sunki mandarin and the Cravo FCAV Rangpur lime. A third cluster of similar rootstocks included the Sun Chu Sha Kat mandarin and the Orlando tangelo which, in general, induced a lower horticultural performance to the Folha Murcha scion. In this study, the Cravo Limeira Rangpur lime and the Flying Dragon trifoliate had unique effects over the Folha Murcha trees, different from the other evaluated rootstocks. 4. Discussion Under the experimental conditions, larger cumulative yield of non-irrigated Folha Murcha trees budded onto Rubidoux trifoliate, Cravo FCAV Rangpur lime and Swingle citrumelo partially confirm previous reports on the effects of Cravo Rangpur lime and Swingle citrumelo, as rootstocks conferring medium to high yields to Folha Murcha and other late-maturing sweet orange cultivars (Stenzel et al., 2005; Castle et al., 2010). The lower cumulative yield of Folha Murcha trees onto Flying Dragon trifoliate is attributed to the reduced tree size induced by this rootstock. Yet, the low cumulative yield and the largest canopy volume of Folha Murcha trees budded onto the Orlando tangelo are attributed to the lowest yield efficiency conferred by this rootstock (Mourão Filho et al., 2007; Cantuarias-Avilés et al., 2010). The Flying Dragon trifoliate rootstock induced early-bearing on Folha Murcha sweet orange, as confirmed by the larger percentage of cumulative yield observed onto this rootstock at the second commercial harvest. In this study, the Orlando tangelo induced a delayed beginning of fruit bearing to Folha Murcha sweet orange. A similar delay on fruit bearing as induced by the Orlando tangelo has been previously described for Hamlin sweet oranges (Pompeu Júnior et al., 2003), Satsuma Okitsu mandarin (Cantuarias-Avilés et al., 2010) and Magallanes pummelo (Odtojan, 1987). Higher alternate bearing indexes of Folha Murcha trees budded onto the Cravo Swingle hybrid and the Sun Chu Sha Kat mandarin contrast with the lowest index recorded onto the Cravo FCAV Rangpur lime. This result partially confirms a study of rootstock performance for the Folha Murcha scion conducted in the Northwest of Paraná State, where the Cravo Rangpur lime and Volkamer lemon rootstocks induced lower alternate bearing to this scion (Stenzel et al., 2005). Higher drought tolerance of Folha Murcha trees budded onto Cravo FCAV, Cravo Limeira Rangpur limes and Sunki mandarin confirms previous reports of the suitability of these rootstocks for non-irrigated conditions (Stuchi et al., 2000b). The high correlation obtained in this study between the three measured leaf colorimetric variables and the scores of visual drought tolerance evaluation, supports the utilization of the colorimetric technique as an accurate and direct method for assessing the intensity of canopy water deficit in Folha Murcha sweet orange trees. A high correlation between leaf water potential and colorimetric variables was also found for Washington Navel sweet orange trees (Deidda et al., 1996). Higher yield efficiency conferred to Folha Murcha sweet orange by the Flying Dragon and FCAV trifoliate rootstocks is consistent with previous results on the effect of trifoliate rootstocks on sweet oranges (Pompeu Júnior et al., 1997; Stenzel et al., 2005; Castle et al., 2007). The Flying Dragon trifoliate rootstock induces the formation of a larger fruit mass per unit of canopy volume (Ferguson et al., 2004), with less non-productive wood distributed into a smaller canopy volume (Richardson et al., 2002), a fact that accounts for its outstanding productive performance. Higher yield efficiency and low vigor of Folha Murcha trees grafted onto Flying Dragon are important advantages for highdensity planting systems. A 4 m 1 m spacing (2500 trees ha 1 ) might cause a 7-fold yield increase on Folha Murcha trees, as compared to a 7 m 4 m spacing (357 trees ha 1 ). However, the low drought tolerance induced by this rootstock (Stuchi et al., 2003) restricts its establishment to the availability of supplementary irrigation. In 2008, the lower CVC incidence on Folha Murcha trees grafted onto the Flying Dragon trifoliate may be explained by a delayed scion bud break in the early spring, as induced by this rootstock. Delayed bud break during the dominant spring flush has been also observed on Silverhill mandarins (Richardson et al., 2002) and Valencia sweet oranges (Bordignon et al., 2003) grafted onto Poncirus trifoliata rootstock. Under non-irrigated conditions, the delayed bud break of Folha Murcha trees grafted onto Flying Dragon trifoliate in the early spring is likely attributed to the higher susceptibility of this rootstock to severe winter drought conditions. Hence, a lag between the presence of young vegetative shoots

7 264 T. Cantuarias-Avilés et al. / Scientia Horticulturae 129 (2011) Fig. 3. Dendrogram of cluster analysis obtained by the single linkage method showing the similarity among groups of rootstocks based on their performance for 14 horticultural variables of Folha Murcha sweet orange budded onto 12 rootstocks. and the occurrence of population peaks of the X. fastidiosa vector sharpshooters feeding on these shoots, may explain the lower CVC incidence observed on trees grafted onto the Flying Dragon trifoliate. This hypothesis was further corroborated in the spring of 2008 (October), when shorter vegetative flushes were observed in Folha Murcha trees grafted onto Flying Dragon trifoliate, as compared to the trees grafted onto Cravo Limeira Rangpur lime (data not shown). Lower CVC susceptibility of Folha Murcha sweet orange trees on the Flying Dragon rootstock was only observed under non-irrigated conditions. In the same experimental site, neither a delayed bud break nor a lower CVC incidence were observed on irrigated Hamlin, Natal and Valencia sweet orange trees budded onto Flying Dragon rootstock (data not shown). Larger fruit weight and lower TSS, TA and TI contents of Folha Murcha sweet oranges grafted onto Cravo FCAV and Cravo Limeira Rangpur limes corroborate previous results on the lower fruit quality induced to this scion by the Rangpur lime rootstock (Stenzel et al., 2005). Larger juice contents were assessed in fruits sampled from trees grafted onto FCAV trifoliate, Cravo Limeira Rangpur lime and Sunki mandarin. From these rootstocks, the FCAV trifoliate conferred high TSS and TI values to the fruits, thus confirming the positive effect of trifoliate rootstocks on Folha Murcha fruit quality (Stenzel et al., 2005). Larger maturation index values associated to earlier fruit ripening of Folha Murcha sweet oranges were observed onto the Cravo Limeira Rangpur lime and the Changsha English Small rootstocks. A similar effect was observed in Hamlin sweet oranges budded onto Changsha English Small in East-Central Florida (Wustcher and Hill, 1995). A multivariate cluster analysis identified both the Flying Dragon trifoliate and the Cravo Limeira Rangpur lime rootstocks as inducing unique effects on Folha Murcha sweet orange horticultural performance. Nevertheless, these rootstocks induced opposite effects on the scion. While the Flying Dragon trifoliate conferred larger yield efficiency, early-bearing and high fruit quality, the Cravo Limeira Rangpur lime induced lower yield efficiency, delayed fruit bearing and low fruit quality to Folha Murcha trees. These results partially confirm a previous study conducted in northwestern Paraná State, describing a distinct effect of the trifoliate rootstock on Folha Murcha tree performance under different groundcover management systems, by using multivariate analyses (Fidalski et al., 2007). Cantuarias-Avilés et al. (2010) also reported a unique effect of Flying Dragon trifoliate on Satsuma Okitsu mandarin, using a hierarchical cluster analysis. 5. Conclusions The Flying Dragon trifoliate rootstock induced smaller tree size, higher yield efficiency, lower CVC incidence, early-bearing and high fruit quality to non-irrigated Folha Murcha sweet orange trees, and may be recommended as an alternative rootstock, being better suited for high-density plantings. The Cravo Limeira and Cravo FCAV Rangpur limes induced early-ripening and larger fruit size, of lower internal quality. The Orlando tangelo performed poorly as rootstock for the Folha Murcha scion, inducing lower yield efficiency, smaller fruit size and lower kg SST box 1. Acknowledgements The authors acknowledge Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the Ph.D. student fellowship to the first author (Proc. 05/ ) and grant support to this research (Proc. 04/ ). The second and third authors acknowledge Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research fellowships. The authors thank Centro APTA Citros Sylvio Moreira for kindly providing part of the germplasm material for the experiment. The authors also acknowledge Mr. Luiz Gustavo Parolin and Mr. Dimas Alves Toledo for technical support, Dr. Jorgino Pompeu Junior for his suggestions during the planning of the experiment, and Dr. Jay L. Schell for critical comments. References Bordignon, R., Medina Filho, H.P., Siqueira, W.J., Pio, R.M., Características da laranjeira Valência sobre clones e híbridos de porta-enxertos tolerantes á tristeza. Bragantia 62,

8 T. Cantuarias-Avilés et al. / Scientia Horticulturae 129 (2011) Bové, J.M., Ayres, A.J., Etiology of three recent diseases of citrus in São Paulo State: sudden death variegated chlorosis and Huanglongbing. IUBMB Life 59, Cantuarias-Avilés, T., Mourão Filho, F.A.A., Stuchi, E.S., Silva, S.R., Espinoza-Nunez, E., Tree performance and fruit yield and quality of Okitsu Satsuma mandarin grafted on 12 rootstocks. Scientia Horticulture 123, Cao, T., Connell, J., Wilhelm, M., Kirkpatrick, B., Influence of inoculation date on the within-plant spread of Xylella fastidiosa and persistence of almond leaf scorch among almond cultivars. Plant Disease 94, doi: /pdis Castle, W.S., Baldwin, J.C., Muraro, R.P., Hamlin orange trees on Flying Dragon trifoliate orange Changsha mandarin, or Koethen sweet orange Rubidoux trifoliate orange citrange rootstock at three in-row spacings in a flatwood site. In: Proceedings of the Florida State Horticultural Society, 120, pp Castle, W.S., Baldwin, J.C., Muraro, R.P., Littell, R., Performance of Valencia sweet orange trees on 12 rootstocks at two locations and an economic interpretation as a basis for rootstock selection. HortScience 45, Cavalcante, I.H.L., Martins, A.B.G., Stuchi, E.S., Campos, M.C.C., Fruit maturation as a parameter for selection of sweet orange cultivars in Brazil. Journal of Food, Agriculture and Environment 7, De Negri, J.D., Blasco, E.E.A., Planejamento e implantação de um pomar cítrico. In: Rodriguez, O., Viégas, F., Pompeu Júnior, J., Amaro, A.A. (Eds.), Citricultura Brasileira., second ed. Fundação Cargill, Campinas, pp Deidda, P., Spano, D., Arca, B., Ventura, A., Duce, P., Colorimetric analysis for determining leaf water status in Citrus. In: Proceedings 8th International Citrus Congress, pp Denecke, A., Temporal and spatial analyses of citrus variegated chlorosis and coffee leaf scorch caused by Xylella fastidiosa. PhD Thesis, Gottfried Wilhelm Leibniz Universität, Hannover, Germany, p EMBRAPA, Centro Nacional de Pesquisa de Solos. Sistema Brasileiro de Classificação de Solos, Rio de Janeiro, p Ferguson, J.J., Chaparro, J., Spann, T.M., Dwarfing and freeze hardiness potential of trifoliate orange rootstocks. IFAS Extension Bulletin HS982, 6. Fidalski, J., Scapim, C.A., Stenzel, N.M.C., Dissimilaridade de porta-enxertos da laranjeira Folha Murcha sob dois sistemas de manejo de cobertura permanente do solo. Revista Brasileira de Ciência do Solo 31, FNP Consultoria e Comércio, Agrianual: Anuário da Agricultura Brasileira. FNP, São Paulo, p Hodgson, R.W., Horticultural varieties of citrus. In: Reuther, W., Batchelor, L.D., Webber, H.J. (Eds.), The Citrus Industry 6. University of California, Berkeley, pp Leite, R.P., Mohan, S.K., Integrated management of the citrus bacterial canker disease caused by Xanthomonas campestris pv. citri in the State of Paraná, Brazil. Crop Protection 9, 3 7. Manly, B.F.J., Multivariate Statistical Methods: A Primer, third ed. Chapman & Hall, London, p Mattos Júnior, D., De Negri, J.D., Pio, R.M., Pompeu Júnior, J. (Eds.), Citros. Instituto Agronômico/FUNDAG, Campinas, p Molina, R.O., Gonçalves, A.M.O., Zanutto, C.A., Nunes, W.M.C., Populational fluctuation of vectors of Xylella fastidiosa Wells in sweet orange (Citrus sinensis (L.) Osbeck) varieties of Northwest Paraná State, Brazil. Brazilian Archives of Biology and Technology 53, Mourão Filho, F.A.A., Espinoza-Núñez, E., Stuchi, E.S., Ortega, E.M.M., Plant growth, yield, and fruit quality of Fallglo and Sunburst mandarins on four rootstocks. Scientia Horticulturae 114, Odtojan, R.C., Rootstock scion relationship study of Magallanes pummelo. Bago-Oshiro, Davao City: BPI, 1; 1987, 13p. details.php?uid=86f1ab348de5b0a fcbb0245 (accessed ). Pompeu Júnior, J., Figueiredo, J.O., Laranjeira, F.F., Behavior of Valencia sweet orange grafted on trifoliate hybrids in São Paulo State Brazil. In: Proceedings of the 5th ISCN International Congress, pp Pompeu Júnior, J., Blumer, S., Salibe, A.A., Tangerinas e tangelos como portaenxertos para a laranja Hamlin. Laranja 24, Richardson, A., Mooney, P., Anderson, P., Dawson, T., Watson, M., How do rootstocks affect canopy development? nz/publications/science/r/richardson/rootcan.htm (accessed ). Stenzel, N.M.C., Neves, C.S.V.J., Gomes, J.C., Medina, C.C., Performance of Ponkan mandarin on seven rootstocks in Southern Brazil. Hortscience 38, Stenzel, N.M.C., Neves, C.S.V.J., Scholz, M.B.S., Gomes, J.C., Comportamento da laranjeira Folha Murcha em sete porta-enxertos no Noroeste de Paraná. Revista Brasileira de Fruticultura 27, Stuchi, E.S., Donadio, L.C., Sempionato, O.R., 2000a. Avaliação da laranjeira Folha Murcha (Citrus sinensis (L.) Osbeck) sobre dez porta-enxertos em Bebedouro, SP. Revista Brasileira de Fruticultura 22, Stuchi, E.S., Donadio, L.C., Sempionato, O.R., 2000b. Tolerância à seca da laranjeira Folha Murcha em 10 porta-enxertos. Revista Brasileira de Fruticultura 22, Stuchi, E.S., Donadio, L.C., Sempionato, O.R., Performance of Tahiti lime on Poncirus trifoliata var. montrosa flying dragon on four densities. Fruits 58, Wustcher, H.K., Hill, L.L., Perfomance of Hamlin orange on 16 rootstocks in East-Central Florida. HortScience 30, Zekri, M., Citrus rootstocks affect scion nutrition, fruit quality, growth, yield and economical return. Fruits 55,