Effect of Phosphonate Applications, for conditions are often prevalent in the cooler, winter rainfall citrus produc- Phytophthora Brown Rot Control, on tion areas of South Africa. ‘Nador- cott’ mandarin trees are known to ‘Nadorcott’ Mandarin External Fruit Quality bear heavily, resulting in branches bending down under the fruit weight, 1,2,4 1 1,3 with numerous fruit often hanging Jan van Niekerk , Charl Kotze , Jade North , close to the orchard floor (J. Joubert, and Paul Cronje1,3 personal communication). This char- acteristic and the fact that it matures during June–August, when rain often ADDITIONAL INDEX WORDS. Phytophthora nicotianae, Phytophthora citrophthora, occurs in the aforementioned pro- phytotoxic damage, ammonium phosphite, potassium phosphite duction areas, leads to the increased SUMMARY. Phosphonate foliar applications in the period before harvest are routinely risk of severe brown rot epidemics used in citrus (Citrus sp.) production for the control of phytophthora brown rot occurring in mandarin orchards. (Phytophthora sp.) control. However, several grower reports indicated that these Properly timed foliar applica- applications caused phytotoxic damage on ‘Nadorcott’ mandarin (Citrus reticulata tions with phosphonates have been hybrid) fruit. To investigate this, trials were conducted over two seasons (2016 and shown to be an excellent preventa- 2017) in two climatically different citrus production areas of South Africa. These tive control measure for brown rot trials consisted of ammonium and potassium phosphite foliar applications (at full of citrus fruit and root rot incited dose or half dose) at green, color break, or full color stages of fruit development. At by Phytophthora species (Graham, commercial harvest, fruit was sampled from the different treatments and the incidence of the phytotoxic damage was documented as both percentage incidence 2011). For brown rot control in and a phytotoxic index (PI). Results indicated that, regardless of the type of South Africa, it is specifically recom- phosphonate or dosage applied, phytotoxic damage was observed at harvest if foliar mended to be applied 1 month or less applications were carried out at color break or full color stage of fruit development. before harvest (Van Zyl, 2017). Phos- The same results were observed in the different climatic areas, although the mean phonates are easily absorbed by the percentage of damaged fruit varied between the areas. Based on these results it is leaves of citrus trees from where they recommended that skirt pruning be used to mitigate phytophthora brown rot on are translocated through the phloem ‘Nadorcott’ mandarin fruit. to sinks, such as developing fruit and roots (Graham, 2011; Ouimette and n 2015, soft citrus (easy peelers) reduce yield, fruit quality, or both Coffey, 1990). At the sites where they made up 9335 ha of the 68,000 in the orchard or in the postharvest accumulate, they have been shown to Iha within the South African citrus cold chain (Adaskaveg et al., 2015; have a direct fungistatic effect on in- industry and is expected to signifi- Montenegro et al., 2008). The dis- vading pathogens and activating the cantly increase in the next 10 years. ease is especially severe in areas where plant’s own defense mechanisms Within this group, late mandarin ac- rainfall occurs during the late stages (Afek and Sztejnberg, 1988, 1989; count for 6560 ha and has earned of fruit development and maturation Fenn and Coffey, 1984, 1985; Smillie growers in 2015 a gross income of (Adaskaveg et al., 2015). et al., 1989). more than R11,000 (South African Propagules of the aforemen- This direct and indirect control Rand) per tonne (South African Cit- tioned two pathogens are present in action combined with a maximum rus Growers Association, 2016). Any most orchard soils, from where they preharvest interval of 28 d makes disease that reduces yield and fruit are readily splashed onto low-hanging late-season phosphonate applications quality can, therefore, greatly affect citrus fruit. Sporangia form on the an attractive option for citrus growers the profitability of this high value low-hanging fruit from where they who are expecting rain close to har- cultivar. In South Africa, brown rot can be splash-dispersed to fruit higher vest that could trigger a brown rot of fruit is primarily incited by Phytoph- up on the tree (Graham et al., 1998; epidemic incited by P. nicotianae thora nicotianae or Phytophthora Timmer et al., 2000). Brown rot (warmer production areas) or P. cit- citrophthora (Meitz-Hopkins et al., epidemics are further promoted by rophthora (cooler production areas) 2013). It is a disease that can severely periods of prolonged wetness (more (Hardman and Hattingh, 2016). than 7 d) and temperatures ranging However, an increasing number of The authors wish to thank Citrus Research Interna- between 23 and 32 C (Graham et al., reports were made by growers in tional for funding of this research and the growers in Nelspruit (Indigo Farming), Riviersonderend and 1998; Timmer et al., 2000). These cooler, winter rainfall, production Riebeek-Kasteel (Suiderland Boerdery) for access to orchards for trial purposes. 1Citrus Research International, P.O. Box 28, Nelspruit 1200, South Africa Units 2Citrus Research International, Department of Plant To convert U.S. to SI, To convert SI to U.S., Pathology, University of Stellenbosch, Private Bag multiply by U.S. unit SI unit multiply by X1, Matieland 7602, South Africa

3 0.4047 acre(s) ha 2.4711 Citrus Research International, Department of Hor- 3.7854 gal L 0.2642 ticultural Science, University of Stellenbosch, Private –1 Bag X1, Matieland 7602, South Africa 0.001 ppm g L 1000 0.1 ppm mL/100 L 10 4 Corresponding author. E-mail: [email protected]. 0.9072 ton(s) tonne(s) 1.1023 https://doi.org/10.21273/HORTTECH04022-18 (F – 32) O 1.8 F C(C · 1.8) + 32

470 • August 2018 28(4) areas of South Africa that they are majority (38%) of the mandarin plant- to only spray single trees. The applica- experiencing phytotoxic damage to ings in South Africa (South African tion times coincided with the imma- mandarin fruit when they applied Citrus Growers Association, 2016). ture green, color break and full color phosphonates at late fruit develop- Different trial sites were selected stages of fruit development. Treat- mental stages, when color develop- for this study to determine whether ments were the same at both sites ment is advanced. As this was the first climatic conditions; i.e., subtropical although a single buffer tree was left of the reports of such damage on (summer rainfall) or Mediterranean between treatments. mandarin fruit, further investigation (winter rainfall) during fruit develop- In the second season (2017), the was warranted. ment played any role in the fruit’s treatments at both sites were the same Le Roux (2000) reported that susceptibility to phytotoxic damage as applied in 2016. However, two foliar sprays of phosphonates can or if it was related to this specific additional treatments were added. cause phytotoxic damage to citrus cultivar. Apart from the label dosages, both leaves and rapidly developing fruit in The first trial site (2016 and potassium phosphite and ammonium the late season if the application rates 2017) was located outside Nelspruit phosphite were also applied at half the are high, as well as if spraying is in the Mpumalanga Province of recommended dosages; i.e., 285 carried out at high ambient tempera- South Africa, which is characterized mL/100 L water for potassium phos- tures or if the treated trees are under by little or no rain during the ‘Nador- phite and 333 mL/100 L water for drought stress. However, investiga- cott’ harvest period in winter. The ammonium phosphite. These addi- tion of the reports from growers trees in this orchard were 10 years old tional treatments were replicated in indicated that label recommendations and planted on Carrizo citrange (Cit- the same manner as the full rate regarding application conditions, tim- rus sinensis · Poncirus trifoliata) treatments. ing and dosages were strictly adhered rootstock. to, thereby, eliminating these as pos- In 2016, the second trial site was Experimental layout sible causes for the observed damage. located at Riviersonderend in the In 2016, the experimental layout However, Walker (1989) reported in- Western Cape Province of South at both sites was a randomized block cidences of phytotoxic damage to Africa. This area is prone to rain, split plot design, with 18 trees within leaves of small, nonfruiting mandarin and, therefore, at a high risk for each block. The main plot factor was trees treated with foliar phosphonate brown rot development, during the chemical treatment (potassium phos- sprays and that the damage increased ‘Nadorcott’ harvest period. This or- phite, ammonium phosphite and un- with increasing dosages. Further- chard was 12 years old and planted on sprayed control) replicated in three more, Manrakhan et al. (2015) found Carrizo citrange rootstock. The sec- blocks and the subplot factor was similar damage on ‘Nadorcott’ man- ond trial site in 2017 had similar application time (different fruit color darin fruit when spinosad-based bait climatic characteristics to Rivierson- development stages—immature green, sprays were applied for the control of derend but was near Riebeek-Kasteel color break, and full color stage). An fruit flies (Ceratitis sp.). In this study, and was a 10-year-old orchard on experimental unit consisted of 40 it was found that damage only oc- Carrizo citrange rootstock. The switch fruit that were harvested randomly curred on fruit that were at the imma- in the trial site was necessitated be- at commercial maturity from the two ture green and color break stage. cause of a severe drought experienced trees of each treatment · application These findings, therefore, indicate a at Riviersonderend in 2017. This could time combination within each block possible change in susceptibly due to have led to trial trees being stressed, replication. changes occurring during maturation which could have adversely affected The 2017 layout was the same of the rind. results obtained. except for two chemical treatments As stated previously, phospho- (half dosages for potassium and am- nate foliar applications in the period Treatments monium phosphite) that were added close to harvest are highly effective for In the first season (2016), potas- to the main plot. the control of phytophthora brown rot sium phosphite [555 gL–1 a.i. (350 EVALUATION OF PHYTOTOXICITY. (Graham, 2011). The aim of this study gL–1 phosphorous acid equivalent) The incidence of the phytotoxic dam- was to verify and quantify any possi- (Fighter; Agchem, Pretoria, South age was documented as both percent- ble phytotoxic damage to ‘Nadorcott’ Africa)] and ammonium phosphite age incidence and a PI for each group mandarin fruit caused by phosphonate [386 gL–1 a.i. (300 gL–1 phospho- of 40 fruit. This dual recording foliar applications, aimed at phytoph- rous acid equivalent) (Brilliant; Arysta resulted in a better understanding of thora brown rot control, at various LifeScience, Umhlanga, South Africa)] not only the incidence of damage per fruit developmental stages, over two were applied according to label rates treatment, as expressed by mean per- seasons (2016 and 2017) in two or- to treated trees. In the case of the centage damaged fruit, but also the chards, located in climatically diverse potassium phosphite, it was 570 mL/ severity of the damage on the indi- production areas. 100 L water and for ammonium phos- vidual fruit as expressed as an index. phite the rate was 666 mL/100 L In the laboratory, the fruit were Materials and methods water with trees sprayed from both evaluated for phytotoxic damage Cultivar and trial sites sides to just before the point of according to a 0 to 3 index which ‘Nadorcott’ mandarin was used runoff, 10 L per tree. A motorized was quantified as a rating; 0 being as all reports of phosphonate phyto- backpack mist blower (Stihl SR 420; fruit with no damage, rating 1 fruit toxic damage occurred on fruit of this Andreas Stihl, Pietermaritzburg, South with <10% of fruit surface damaged, cultivar. It furthermore makes up the Africa) was used for all applications rating 2 fruit having 11% to 30%

• August 2018 28(4) 471 RESEARCH REPORTS surface damaged, and a rating 3 where with either potassium or ammonium treatment x color phase interaction. fruit with >30% of the fruit surface phosphite. On fruit that was sprayed At both trial sites, no damaged fruit displayed damage. with these chemicals at color break was observed at harvest when potas- phase, the phytotoxic damage on the sium phosphite was sprayed at the 9 PI = S ½rind damage severityðÞ 0 3 fruit rind manifested as dark brown green stage (Table 1; Fig. 1). Al- number of fruit within each class lesions of variable sizes (Fig. 2A and though not significantly higher, com- = : B). These lesions consisted of an pared with potassium phosphite 0.2% total number of fruit area where the flavedo was damaged damaged fruit was observed at har- to such an extent that the white, vest, at both trial sites, on fruit At each application time, a sample of underlying albedo was exposed. A sprayed with ammonium phosphite 20 fruit were collected. The fruit rind green margin was furthermore ob- at the green stage. However, this color of these fruit was measured, to served to occur around the lesions was not significantly more than the determine the fruit color at the differ- (Fig. 2A and B). unsprayed control (Table 1). For this ent application times and to indicate On fruit that was sprayed with application, the average PI on the the change in rind color develop- the aforementioned chemicals at the 0.2% damaged fruit was less than ment between application times. The full color developmental phase (Fig. 0.05, indicating that very slight dam- measurements were carried out with 2C and D), much more severe dam- age had occurred (Table 1). a chroma meter (CR-400; Konica age was observed of the fruit rind However, for fruit sprayed at the Minolta Sensing, Osaka, Japan) on compared with fruit sprayed at the color break stage, significant differ- the sun-exposed side of each fruit green stage (not shown). Again, the ences compared with the control were and expressed by the Hunter a/b ratio lesions were of variable sizes but had observed between the trial sites, irre- (Fig. 1). the appearance of dark brown, sunken spective of the chemical applied (Ta- STATISTICAL ANALYSIS. Data were areas, where the flavedo was damaged ble 1). At the Riviersonderend trial subjected to analysis of variance and the underlying albedo had a red- site, no fruit were damaged by either (ANOVA) according to the experi- dish brown color (Fig. 2C and D). of the chemicals when applied at the mental design using SAS (version 9.3; PERCENTAGE INCIDENCE AND color break stage. Compared with SAS Institute, Cary, NC). Experi- SEVERITY OF PHYTOTOXIC DAMAGE. this, at the Nelspruit trial site, a mean mental results from the two sites Analysis of variance of the mean per- percentage of 44.2% was damaged by were also combined after confirma- centage fruit with phytotoxic damage potassium phosphite applications at tion of site homogeneity of variance. in 2016 indicated a significant [P < color break stage. The average PI of Where site variances were unequal 0.001 (ANOVA not shown)] area x this fruit was 1.23 (Table 1). A mean (2017data)aweightedANOVA was conducted. Fisher’s least signif- icant difference was calculated at a 5% significance level to compare means. Results Phytotoxic damage symptoms At trial evaluation, in both years, similar symptoms of phytotoxic dam- age were observed on fruit sprayed

Fig. 1. Graphic representations of the color change in the ‘Nadorcott’ mandarin fruit at the various treatment application dates between Fig. 2. Phytotoxic damage caused on the rind of ‘Nadorcott’ mandarin fruit at April and August. Color change is harvest after potassium or ammonium phosphite applications (full or half dose) at expressed as the Hunter a/b ratio. color break (A, B) or full color (C, D) stage of fruit development.

472 • August 2018 28(4) percentage of 40% was damaged by notably more than the unsprayed The application with half dose ammo- ammonium phosphite applications at control (Table 1). nium phosphite caused a mean per- the same stage resulting in an average Analysis of the 2017 data indi- centage of damaged fruit of 21. 7% PI of 1.12 (Table 1). For the respec- cated only a significant (P < 0.001) that was statistically similar to the tive chemicals these mean percentages treatment x color phase interaction other treatments, except the full were statistically similar but signifi- (ANOVA not shown). In terms of the dose potassium phosphite applica- cantly more than the unsprayed treat- incidence of damage observed, am- tion (Table 2). In terms of the se- ment where no damaged fruit was monium phosphite applications at verity, the most severe damage (PI observed (Table 1). half dose during the green phase, 1.07) was also caused by the full- The results obtained with full caused 1.7% fruit to show phytotoxic dose potassium phosphite application. color applications again indicated sig- damage at harvest. However, the PI This was similar to the half-dose potas- nificant differences between the areas of this fruit was only 0.03 (Table 2) sium phosphite application (PI 0.70) and the two chemicals tested. At the and the percentage damaged fruit was and full-dose ammonium phosphite Riviersonderend trial site 100.0% of not significantly higher than the other application (PI 0.70). The latter two fruit sprayed with potassium phos- chemical treatments or the unsprayed treatments did, however, not cause phite at this stage showed damage control where no damage was ob- notably more severe damage than the with a high PI of 2.36 (Table 1). This served (Table 2). half-dose ammonium phosphite appli- application in Nelspruit caused signif- At the color break phase, the cation [PI 0.33 (Table 2)]. icantly less damage at 85.0% although potassium phosphite and ammonium Significant increased incidence the PI of 2.33 did not differ much phosphite applications, at full and half of damage occurred in fruit in all from that observed at Riviersonder- dosages, caused phytotoxic damage treatments when applied at the full end (Table 1). The ammonium phos- that was significantly more than the color stage (Table 2). The highest phite applications at the two sites unsprayed control (Table 2). The full incidence of damage was seen with resulted in statistically similar inci- dose potassium phosphite application the full dose of potassium phosphite dences of 93.3% in Riviersonderend caused a mean percentage of dam- applications; i.e., 63.3% and PI of and 95.0% in Nelspruit. Furthermore, aged fruit of 59.2% that was, although 1.11. This percentage damage was the PI of this application at the dif- not significant, more than potassium statistically similar to the full-dose ferent sites were similar at 2.69 and phosphite applied at half dose (40.0%) ammonium phosphite applications 2.58, respectively, and not in all cases and ammonium phosphite (39.2%). (52.5%) with a PI of 1.11, which

Table 1. Mean percentage damaged fruit observed at harvest after potassium and ammonium phosphite treatments applied at the green, color break, and full color stages of ‘Nadorcott’ mandarin fruit development in 2016 at the Riviersonderend and Nelspruit, South Africa, trial sites. Average phytotoxic index (PI) values are presented in parenthesis. Riviersonderend Nelspruit Color phase Green Color break Full color Green Color break Full color Treatment Mean damaged fruit (%) (Avg. PI)z Potassium phosphite 0.0 ey (0.00) 0.0 e (0.00) 100 a (2.36) 0.0 e (0.00) 44.2 d (1.23) 85 c (2.33) Ammonium phosphite 0.2 e (0.00) 0.0 e (0.00) 93.3 b (2.70) 0.2 e (0.00) 40 d (1.12) 95 ab (2.58) Unsprayed 0.0 e (0.00) 0.0 e (0.00) 0.0 e (0.00) 0.0 e (0.00) 0.0 e (0.00) 0.0 e (0.00) LSD value 5.207 zAverage phytotoxic rating calculated per experimental unit of 40 fruit. y Means with a different letter within a column differ significantly at the 5% level via Fisher’s least significant difference (LSD).

Table 2. Mean percentage damaged fruit observed at harvest caused by full- and half-dose potassium and ammonium phosphite treatments applied at the green, color break, and full color stages of ‘Nadorcott’ mandarin fruit development in 2017 at the Riebeek-Kasteel and Nelspruit, South Africa, trial sites. Average phytotoxic index (PI) values are presented in parenthesis. Color phase Green Color break Full color Treatment Mean damaged fruit (%) (Avg. PI)z Potassium phosphite (full dose) 0.00 f y (0.00) 59.17 ab (1.07) 63.33 a (1.11) Potassium phosphite (half dose) 0.00 f (0.00) 40.00 bcd (0.70) 20.83 de (0.37) Ammonium phosphite (full dose) 0.00 f (0.00) 39.17 bcd (0.70) 52.50 ab (0.92) Ammonium phosphite (half dose) 1.67 ef (0.03) 21.67 cde (0.33) 41.67 bc (0.85) Unsprayed 0.00 f (0.00) 0.00 f (0.00) 0.00 f (0.00) LSD value 20.41 zAverage phytotoxic rating calculated per experimental unit of 40 fruit. y Means with a different letter within a column differ significantly at the 5% level via Fisher’s least significant difference (LSD).

• August 2018 28(4) 473 RESEARCH REPORTS was markedly higher than the half- develop into reddish brown areas. and hemicellulose also get broken dose treatments or untreated control However, unlike rind breakdown, down that reduce firmness while treatment (Table 2). The half-dose the phytotoxic lesions observed were ripening (Muramatsu et al., 1999). ammonium phosphite application had not randomly distributed on the fruit These changes potentially could an incidence of 41.7% damaged fruit surface but were mostly on the ex- make the fruit more susceptible not with a PI of 0.85. The half-dose po- posed side or at the bottom of the only to physical but also to chemical tassium phosphite application at color fruit due to droplet runoff. This type damage, as the mandarin fruit break caused the least amount of dam- of symptom development was espe- matures. age with an incidence of 20.8% and PI cially seen with applications carried It is, therefore, possible that the of 0.37, both values significantly the out at full color stage (Figs. 1 and 2C, phytotoxic damage of the rind by lowest (Table 2). D). It is suspected that the lesion phosphonate applications as seen in development after cellular collapse, this study was incited by one of two Discussion after phosphonate foliar applications mechanisms. After application at ei- Results from the present study, follows the same progression in de- ther color break or full color stage, carried out over 2 years in climatically velopment of brown discoloration as the phosphonates are easily absorbed diverse production areas, clearly in- during rind breakdown. Degradation into the rind where it can either cause dicated that irrespective of application of cells combined with enzymatic direct damage to the flavedo damag- dosage (full or half), phytotoxic dam- oxidation of the phenolic rich vacuo- ing either the oil cells or adjacent age of ‘Nadorcott’ mandarin fruit lar contents was regarded as the tissues or both. Damage of the oil occurred when potassium or ammo- cause of the dark brown areas ob- cells will release phytotoxic oils that in nium phosphite foliar applications served during rind breakdown (Agustı turn damages the susceptible underly- were carried out at either the color et al., 2001). Development of rind ing cells. This could lead to release and break or full color fruit developmental pitting in ‘Encore’ mandarin fruit and subsequent oxidation and browning stage. This then also constitutes the oleocellosis in ‘Washington’ navel or- of the vacuolar content. Alternatively, first report of phytotoxic damage by anges (C. sinensis) has been attributed the phosphonates could directly dam- phosphonate foliar spray applications to the release of phytotoxic rind oils age the cells of the flavedo, leading to on ‘Nadorcott’ mandarin fruit. from oil cells in the flavedo that were the release and oxidation of the vacu- Phytotoxic damage of mandarin damaged by environmental or me- olar content. leaves caused by phosphonate appli- chanical damage (Knight et al., 2002; It is of interest to note that cations was previously reported by Medeira et al., 1999). during the first season (2016), signif- Walker (1989). Le Roux (2000) fur- The efficacy of phosphonate ap- icant differences in phytotoxic damage thermore reported that when phos- plications as preventative measures occurred between Riviersonderend phonate foliar applications are carried for the control of root rot and brown and Nelspruit in both incidence (per- out at high dosages, high ambient rot on fruit incited by Phytophthora centage damaged fruit) as well as temperatures, or when trees are under species was attributed to it being severity (PI). No damage was observed stress, phytotoxic damage can occur. easily absorbed by the leaves of cit- in Riviersonderend whereas in Nel- However, phosphonates have been rus trees from where it gets trans- spruit the amount of damage ranged used for many years on other cultivars located in the phloem (Graham, between 40% and 44.2% (Table 1). without causing phytotoxic damage 2011; Ouimette and Coffey, 1990). These variances could be attributed to of fruit. Manrakhan et al. (2015) did Absorption of phosphonates by fruit differences in fruit maturation rates report phytotoxic damage of ‘Nador- could potentially also occur as the between the two areas, which could cott’ mandarin fruit by certain fruit fly citrus rind was described by Schneider have influenced the rind susceptibility. bait sprays. By contrast to the present (1968) as being a modified leaf with A difference in fruit maturation rate study, they reported that damage only stomata remaining active during all between the two areas is furthermore occurred when applications were car- stages of fruit development. supported by the trail evaluation in ried out on fruit at the immature During ripening the fruit rind Riviersonderend taking place during green or color break stage of fruit undergoes several changes that in- July 2016 whereas in Nelspruit this development. These results indicate clude color development through was carried out 4 weeks earlier in June a possible change in the ‘Nadorcott’ the breakdown of chlorophyll and 2016. mandarin rind biochemical composi- synthesis of carotenoids (Iglesias Evident from the results tion during the rind maturation, et al., 2007) as well as carbohydrate obtained in this study is that phos- which resulted in such a dramatic composition and more impor- phonate applications, regardless of change in sensitivity to a chemical. tantly compositional changes of cu- production area climate, cannot be Even though the mechanism of ticularwax,thefirstbarrierwhich used as a means of brown rot control the phytotoxic damage differs com- would affect the uptake of a chemical on late mandarin fruit from color pletely, the observed symptom de- into the flavedo cells (Albrigo, break stage of fruit development until velopment in the present study 1972; El-Otmani and Coggins, harvest. Other measures such as skirt- resembled to some extent the physi- 1987; El-Otmani et al., 1987). In ing of trees should, therefore, be ological rind breakdown seen in addition, and possibly more impor- employed to manage this disease in ‘Navelate’ sweet orange [C. sinensis tantly, are the changes that occur in these cultivars. It is also still possible (Agustı et al., 2001)]. The rind break- the epidermis where cracks develop to use phosphonate foliar or trunk down symptoms were described as as the fruit grows, while certain cell applications as part of a preventative sunken, colorless areas that over time wall components such as cellulose management program for root rot

474 • August 2018 28(4) incited by Phytophthora species, as Fenn, M.E. and Coffey. 1985. Further Meitz-Hopkins, J.C., M.C. Pretorius, C. these applications occur just after fruit evidence for the direct mode of action of F.J. Spies, L. Huisman, W.J. Botha, S.D. set and during the immature green fosetyl-Al and phosphorous acid. Phyto- Langenhoven, and A. McLeod. 2013. Phytophthora stage of fruit development (Le Roux, pathology 75:1064–1068. species distribution in South 2000). African citrus production regions. Eur. J. Graham, J.H. 2011. Phosphite for control Plant Pathol. of phytophthora diseases in citrus: Model for management of Phytophthora species Montenegro, D., O. Aguın, C. Pintos, Literature cited on forest trees? N. Z. J. For. Sci. 41S:S49– M.J. Sainz, and J.P. Mansilla. 2008. A Adaskaveg, J.E., W. Hao, and H. Forster.€ S56. selective PCR-based method for the 2015. Postharvest strategies for managing identification of Phytophthora hibernalis Graham, J.H., L.W. Timmer, D.L. phytophthora brown rot of citrus using Carne. Span. J. Agr. Res. 6:78–84. Drouillard, and T.L. Peever. 1998. potassium phosphite in combination with Characterization of Phytophthora sp. Muramatsu, N., T. Takahara, T. Ogata, heat treatments. Plant Dis. 99:1477– causing outbreaks of citrus brown rot in and K. Kojima. 1999. Changes in rind 1482. Florida. Phytopathology 88:724–729. firmness and cell wall polysaccharides Afek, U. and A. Sztejnberg. 1988. Accu- during citrus fruit development and mat- Hardman, P. and V. Hattingh. 2016. mulation of scoparone, a phytoalexin as- uration. HortScience 34:79–81. Recommended usage restrictions for sociated with resistance of citrus to plant protection products on Southern Ouimette, D.G. and M.D. Coffey. 1990. Phytophthora citrophthora. Phytopathol- African export citrus. Dec. 2016. Citrus Symplastic entry and phloem trans- ogy 78:1678–1682. Research International, Nelspruit, South location of phosphonate. Pestic. Bio- Afek, U. and A. Sztejnberg. 1989. Effects Africa. chem. Physiol. 38:18–25. of fosetyl-Al and phosphorous acid on Iglesias, D.J., M. Cercos, J.M. Colmenero- Schneider, H. 1968. The anatomy of cit- scoparone, a phytoalexin associated with Flores,M.A.Naranjo,G.Rios,E.Carrere, rus, p. 1–85. In: H.J. Weber and L.D. resistance of citrus to Phytophthora cit- O. Ruiz-Rivero, I. Lliso, R. Morillon, and Batchelor (eds.). The citrus industry. rophthora. Phytopathology 79:736–739. F.R.M.T. Tadeo. 2007. Physiology of Univ. California Press, Los Angeles, CA. Albrigo, L.G. 1972. Distribution of sto- citrus fruiting. Braz. J. Plant Physiol. Smillie, R., B.R. Grant, and D. Guest. mata and epicuticular wax on oranges as 19:333–362. 1989. The mode of action of phosphite: related to stem end rind breakdown and Knight, T.G., A. Klieber, and M. Sedgley. Evidence for both direct and indirect water loss. J. Amer. Soc. Hort. Sci. 2002. Structural basis of the rind disorder modes of action on three Phytophthora sp. 97:220–223. oleocellosis in Washington navel orange in plants. Phytopathology 79:921–926. Agustı, M., V. Almela, M. Juan, F. (Citrus sinensis L. Osbeck). Ann. Bot. South African Citrus Growers Associa- Alferez, F.R. Tadeos, and L. Zacarıas. 90:765–773. tion. 2016. Key industry statistics for cit- 2001. Histological and physiological Le Roux, H.F. 2000. Physiological in- rus growers 2016. South African Citrus characterization of rind breakdown of teractions of phosphorous acid and con- Grower’s Assn., Hillcrest, South Africa. ‘Navelate’ sweet orange. Ann. Bot. trol of root pathogens. Proc. Intl. 88:415–422. Citricult. IX Congr. II:926–928. Timmer, L.W., S.E. Zitko, T.R. Gottwald, and J.H. Graham. 2000. Phytophthora El-Otmani, M., M.L. Arpaia, and C.W. Manrakhan, A., P.R. Stephen, and P.J.R. brown rot of citrus: Temperature and Coggins. 1987. Developmental and topo Cronje. 2015. Phytotoxic effect of GF- moisture effects on infection, sporan- physical effects on the n-alkanes of 120 NF fruit fly bait on fruit of mandarin gium production, and dispersal. Plant Valencia orange fruit epicuticular wax. J. (Citrus reticulata Blanco cv. Nadorcott): Dis. 84:157–163. Agr. Food Chem. 35:4246. Influence of bait characteristics and fruit Van Zyl, K. 2017. The chemical control of El-Otmani, M. and C.W. Coggins. 1987. maturity stage. Crop Protection 78:48– plant diseases in South Africa. AVCASA, Fruit age and growth regulator effects on 53. Halfway House, South Africa. the quantity and structure of the epicu- Medeira, M.C., M.I. Maia, and R.F. ticular wax of ‘Washington’ navel orange Vitor. 1999. The first stages of pre-harvest Walker, G.E. 1989. Phytotoxicity in fruit. J. Amer. Soc. Hort. Sci. 110:371– ‘peel pitting’ development in ‘Encore’ mandarins caused by phosphorous acid. 378. mandarin. A histological and ultrastruc- Austral. Plant Pathol. 18:57–59. Fenn, M.E. and M.D. Coffey. 1984. tural study. Ann. Bot. 83:667–673. Studies on the in vitro and in vivo antifungal activity of fosetyl-Al and phosphorous acid. Phytopathology 74: 606–611.

• August 2018 28(4) 475