plants Article Russeting in ‘Apple’ Mango: Triggers and Mechanisms Thomas O. Athoo, Andreas Winkler and Moritz Knoche * Institute of Horticultural Production Systems, Leibniz University Hannover, Herrenhäuser Straße 2, 30419 Hannover, Germany; [email protected] (T.O.A.); [email protected] (A.W.) * Correspondence: [email protected]; Tel.: +49-511-762-9020 Received: 3 July 2020; Accepted: 14 July 2020; Published: 16 July 2020 Abstract: Russeting is an important surface disorder of many fruitcrop species. The mango cultivar ‘Apple’ is especially susceptible to russeting. Russeting compromises both fruit appearance and postharvest performance. The objective was to identify factors, mechanisms, and consequences of russeting in ‘Apple’ mango. Russeting was quantified on excised peels using image analysis and a categorical rating scheme. Water vapour loss was determined gravimetrically. The percentage of the skin area exhibiting russet increased during development. Russet began at lenticels then spread across the surface, ultimately forming a network of rough, brown patches over the skin. Cross-sections revealed stacks of phellem cells, typical of a periderm. Russet was more severe on the dorsal surface of the fruit than on the ventral and more for fruit in the upper part of the canopy than in the lower. Russet differed markedly across orchards sites of different climates. Russet was positively correlated with altitude, the number of rainy days, and the number of cold nights but negatively correlated with minimum, maximum, and mean daily temperatures, dew point temperature, and heat sum. Russeted fruit had higher transpiration rates than non-russeted fruits and higher skin permeance to water vapour. Russet in ‘Apple’ mango is due to periderm formation that is initiated at lenticels. Growing conditions conducive for surface wetness exacerbate russeting. Keywords: Mangifera indica; skin; periderm; cuticle; epidermis; lenticel 1. Introduction Russeting is a surface disorder of many fruitcrop species worldwide. In botanical terms, russet represents the formation of a periderm [1] comprising three layers: a phellogen (meristematic) that gives rise to a phelloderm (to the inside) and a phellem (to the outside). The phellem comprises stacks of cork cells. It is their suberised cell walls that are responsible for the rough, brown appearance of a russeted fruit skin. This appearance is generally unattractive to the consumer [2]. Russet therefore compromises the visual quality of a fruit and thus excludes it from the high-value export markets. Russet is also associated with increased postharvest water loss, which further compromises postharvest performance [3]. This requires fruit cartons to be “overpacked” if they are to reach the end consumer at the pre-specified weight. For both these reasons, russeting has serious economic consequences for the grower. Malus apple is a prominent example of a susceptible fruit crop. Most information on the ontogeny of russet is available for this species. In apple, russet is preceded by the formation of microcracks in the cuticle [4,5]. Surface wetness [6,7], agrichemicals [8,9], and pests and diseases such as mites [10], epiphytic fungi [11], and bacteria [12] are all factors aggravating russeting. A periderm forms, presumably in the hypodermal cell layers [13,14]. The cuticle and the epidermis dry out and slough off as the phellem develops. The brownish cork cells are then revealed on the fruit surface. Plants 2020, 9, 898; doi:10.3390/plants9070898 www.mdpi.com/journal/plants Plants 2020, 9, x FOR PEER REVIEW 2 of 19 oPlantsut and2020 slough, 9, 898 off as the phellem develops. The brownish cork cells are then revealed on the 2fruit of 17 surface. The ‘Apple’ mango is a valuable mango cultivar in the Kenyan market. It has excellent texture and flavour.The ‘Apple’ Unfortunately, mango is a ‘Apple’ valuable mango mango is cultivar also highly in the susceptible Kenyan market. to a skin It has disorder excellent that texture bears similarityand flavour. to the Unfortunately, well-known russet ‘Apple’ of mangomany apple is also and highly pear susceptiblecultivars. To to our a skin knowledge disorder, there that bearsis no informationsimilarity to available the well-known on this disorder russet of in many mango. apple and pear cultivars. To our knowledge, there is no informationThe objective available of this on thisstudy disorder was (1) in to mango. identify whether the “russet” of ‘Apple’ mango is caused by a peridermThe objective formation of this studyand (2) was to (1)identify to identify the agronomic whether the and “russet” the environmental of ‘Apple’ mango factors is causedaffecting by thea periderm incidence formation and severity and of (2) “russeting to identify” in the this agronomic cultivar. and the environmental factors affecting the incidence and severity of “russeting” in this cultivar. 2. Results 2. Results Russet severity in ‘Apple’ mango was non-uniform within a tree and across an orchard. The severityRusset of russet severity in in the ‘Apple’ same mango orchard was ranged non-uniform from non within-russeted a tree and(Figure across 1a, an score orchard. 0) to The moderate severity (Figureof russet 1c, in score the same 2) to orchard extreme ranged (Figure from 1b, score non-russeted 4). The russet (Figure scores1a, score of the 0) to rating moderate scheme (Figure used1 c,to quantifyscore 2) torusset extreme were (Figure closely1b, scorecorrelated 4). The to russet the actual scores russeted of the rating surface scheme area used measured to quantify by russetimage analysiswere closely (Figure correlated 1d). to the actual russeted surface area measured by image analysis (Figure1d). FigureFigure 1. 1. MacroscopeMacroscope view view of ofmature mature ‘Apple’ ‘Apple’ mango mango with withoutout (a, score (a, score 0), moderate 0), moderate (b, score (b, score 2), and 2), extremeand extreme (c, score (c, score 4) russet 4) russet symptoms. symptoms. (d) (: dPlot): Plot of ofrusseting russeting (rating (rating score) score) against against percentage percentage area area affectedaffected by russet (image analysis). Each Each fruit fruit was was rated rated visually visually prior prior to to image image analysis. analysis. The The number number ofof observations observations was 18. FruitFruit surface surface area area increased increased with with time time (Figure (Figure 22a).a). TheThe growthgrowth raterate inin surfacesurface areaarea waswas atat aa 2 1 maximummaximum of of 2.3 cm 2 dayday−−1 atat about about 114 114 days days after after full full bloom bloom (DAFB) (DAFB) and and decreased continuously thereafterthereafter (Figure (Figure 22aa inset).inset). The percentage of the surface area ofof thethe skinskin exhibitingexhibiting russetrusset increasedincreased with time through throughoutout development (Figure 2 2bb,c).,c). Plants 2020, 9, 898 3 of 17 Plants 2020, 9, x FOR PEER REVIEW 3 of 19 Figure 2. Change in in fruit surface area (cm 22)) and and rate rate of of surface surface expansion expansion ( (aa andand aa inset )) with time ((daysdays after full bloom, DAFB). Percent of skin with russet in developing fruit (b)) calculated from from a a defineddefined areaarea ofof the the fruit fruit cheek. cheek. The The same same fruit fruit was was photographed photographed at 100, at 156, 100, and 156 216, and DAFB 216 (seeDAFB arrows). (see arrows).Pictorial representationPictorial representation of russet progressionof russet progression in a developing in a developing ‘Apple’ mango ‘Apple’ fruit mango (c1–c3 ).fruit Scale (c1 bar–c3 is). Scale10 mm. bar Data is 10 represent mm. Data means representSE means of 19 replicates. ± SE of 19 replicates. ± Microscopic ins inspectionpection of of the fruit surface following labelling with acridine orange revealed thatthat initial cracking always began at a lenticel (Figure 33a–d).a–d). LenticelsLenticels rupturedruptured andand developeddeveloped intointo (usually) three-three- or or four-pointed four-pointed star- star or- triangular-shaped or triangular-shaped short cracks.short cracks. These wereThese filled were with filled periderm with periderm(Figure3e–h). (Figure These 3e– stellateh). These cracks stellate enlarged cracks and enlarged merged and as cracks merged propagated as cracks and propagated development and developmentprogressed. They progressed. eventually They formed eventually islands formed of crack islands networks. of crack These networks islands. laterThese expanded islands later and expandedmerged. The and end merged. result was The an extensiveend result network was an of rough,extensive brown network patches. of Occasionally, rough, brown these patches patches. Oextendedccasionally over, these theentire patches fruit extended surface (Figureover the3i–n). entire Only fruit during surface the (Figure initial stages3i–n). Only of cracking during was the initialthere significantstages of cracking infiltration was of there acridine significant orange atinfiltration the lenticels of acridine (Figure3 orangeb,d). There at the was lenticels essentially (Figure no 3b,d).infiltration There after was theessentially periderm no had infiltration developed after (Figure the periderm3h,j,l,n). had developed (Figure 3h,j,l,n). The non-russeted fruit skin had an intact cuticle, epidermis, and hypodermis (Figure4a,b). There was no cuticle or epidermis on the lenticels (Figure4c–j). The pore of the lenticel was filled with stacks of thick-walled cells varying from three layers (initial stage of russeting) to more than five (extreme russeting) (Figure4c–j). The walls of these cells fluoresced following staining with fluorol yellow. This identified them as the suberised (corky) walls of a typical periderm (Figure4d,f,h,j). Plants 2020, 9, 898 4 of 17 Plants 2020, 9, x FOR PEER REVIEW 4 of 19 FigureFigure 3. 3.Microscopic Microscopic view view of of ‘Apple’ ‘Apple’mango mango skinskin infiltratedinfiltrated with with acridine acridine orange orange dye dye when when viewed viewed with a binocular microscope under natural (a,c,e,g,i,k,m) or fluorescent light (b,d,f,h,j,l,n). The scale with a binocular microscope under natural (a,c,e,g,i,k,m) or fluorescent light (b,d,f,h,j,l,n).