Flowering time determines the weight and composition of Actinidia chinensis var. chinensis ‘Zesy002’ kiwifruit

Scientia Horticulturae 246 (2019) 741–748

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Flowering time determines the weight and composition of Actinidia chinensis var. chinensis ‘Zesy002’ kiwifruit

T

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Annette Richardsona, , Helen Boldinghb, Peggy Kashubaa, Georgia Knighta, Deborah Ellinghama a b

The New Zealand Institute for Plant & Food Research Limited (PFR), Kerikeri Research Centre, 121 Keri Downs Road, RD1, Kerikeri, 0294, New Zealand PFR, Ruakura Research Centre, Private Bag 3230, Waikato Mail Centre, Hamilton, 3240, New Zealand

A R T I C LE I N FO

A B S T R A C T

Keywords: Acid Dry matter Flower Kiwifruit Outer pericarp Sugar

Consistently high flavour in fruit of a recently released commercial gold-fleshed kiwifruit cultivar ‘Zesy002’ is important for consumer acceptance. We hypothesised that variation in fruit weight and quality was determined during flower differentiation, and that date of flower opening and flower type (terminal or lateral) were important indicators. We determined whether time of flowering (early 5% open, mid 50% open and late 95% open) and flower type (terminal or lateral) influenced fruit weight, fruit maturity and fruit composition over two growing seasons. Fruit that developed from early-opening terminal flowers were 12–13 g heavier than those that developed from late-opening terminal flowers. Measurements in the second season suggested that this difference in fruit weight was related to ovary weight. Early-opening flowers were produced on shoots from smaller diameter canes than mid- and late-opening flowers. The soluble solids content, firmness and flesh colour of fruit was related to the period of fruit development, so late-opening flowers produced less-mature fruit as kiwifruit are harvested at a single date. Early-opening terminal and lateral flowers had significantly more outer pericarp tissue than fruit that developed from late-opening terminal flowers. This difference in tissue proportion was associated with 1–2 units higher fruit dry matter content and higher sugar:acid ratios in ripe fruit juice. Fruit from earlyopening lateral flowers were smaller but had similar maturity and sugar:acid ratios to fruit from early-opening terminal flowers. These results suggest that competition during flower differentiation in spring influences the weight and composition of the ovary and fruit attributes at harvest. Hence, these attributes of ‘Zesy002’ fruit could be managed by manipulating flower development in spring.

1. Introduction Consumer acceptance of fruit is driven by their appearance and taste. For kiwifruit, fruit weight and flavour indicators, such as sugar and acid concentrations, are key components of consumer acceptance (Crisosto and Crisosto, 2001). Both the mean value and variation in these characteristics affect the consumer response and their willingness to make repeat purchases. Generally the aim of kiwifruit breeding and vine management research is to change the mean value of key traits. However, the variation in these traits can still be large, with variation in fruit characteristics within a single kiwifruit vine as large as the variation across all other layers of the commercial industry (Smith et al., 1994). Yellow-fleshed kiwifruit cultivars have become increasingly important in the international market. ‘Zesy002’ is a new cultivar that replaced the first globally commercialised yellow cultivar Actinidia chinensis var. chinensis ‘Hort16A’ after the debilitating disease

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Pseudomonas syringae pv. actinidiae biovar 3 arrived in New Zealand (Ferguson, 2015). ‘Zesy002’ produces very large fruit, generally with high dry matter contents. In kiwifruit high dry matter contents are correlated with high total soluble solids concentration (SSC) in ripe fruit (Richardson et al., 1997). In kiwifruit, as well as many other fruits including tomato, there is a general trend that as mean fruit weight increases there is a decrease in mean dry matter and sugar content (Prudent et al., 2009; Nardozza et al., 2010). However, the opposite has been observed in a population of ‘Zesy002’ fruit where smaller fruit have lower dry matter contents, risking less favourable consumer responses. Understanding the variation in fruit weight and flavour in a population and how variation develops is important for better management of fruit quality to meet consumer demands. Variation in fruit characteristics within plants has been studied in many fruit crops and is generally related to factors that affect carbohydrate supply to the fruit. Factors that affect carbohydrate supply from the source leaf to the fruit includes the position of fruit on the plant

Corresponding author. E-mail address: [email protected] (A. Richardson).

https://doi.org/10.1016/j.scienta.2018.11.043 Received 6 September 2018; Received in revised form 6 November 2018; Accepted 14 November 2018 0304-4238/ © 2018 Elsevier B.V. All rights reserved.

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(Boyd et al., 2008; Trought et al., 2017), light exposure (Reshef et al., 2017), shoot type and leaf area (Tombesi et al., 1993; Landi et al., 2014; Nardozza et al., 2015). Competition for carbohydrate supply between fruit is affected by fruit crop load (Stanley et al., 2014), flowering date (Fukuda et al., 2015) and flower type on an inflorescence (Lai et al., 1990). In perennial fruit crops, competition for carbohydrate supply begins early in the growing season, before flowering. In kiwifruit, where flower differentiation occurs over an extended period between budbreak and flowering (Brundell, 1975), this competition affects shoot development (Piller et al., 1998). The duration of flowering on kiwifruit vines may vary from a few days to several weeks (McPherson et al., 1994; Richardson et al., 2001) because of environmental effects like winter and spring temperatures (McPherson et al., 2001a), wood and flower type (Richardson et al., 2001) or the use of growth regulators like hydrogen cyanamide (McPherson et al., 2001a). Previous studies have established that early-opening flowers develop into larger fruit than late-opening flowers in kiwifruit (Lai et al., 1990), apple (Denne, 1963) and grape (Coombe, 1980). Many fruit crops like kiwifruit, grape, apple and pear produce flowers in branched inflorescences. Kiwifruit flowers develop in a compound dichasium with a terminal flower, and primary and secondary lateral flowers (Hopping, 1990). In a previous study of ‘Hayward’ kiwifruit, fruit from terminal flowers were larger than those that developed from lateral flowers regardless of the inflorescence configuration, but there was no effect of flower type on fruit maturation or dry matter content (Antognozzi et al., 1991). In this study we investigated how variation in flowers influenced the growth and composition of ‘Zesy002’ kiwifruit during two growing seasons. The aim was to determine whether time of flowering and/or flower type affect final fruit weight, tissue composition, fruit maturation or sugar and acid composition. Our hypothesis was that competition for carbohydrate before flowering affects the ovary weight and subsequent fruit tissue development, and causes variation in ripe fruit composition.

Table 1 Date of flowering and the number of days from flowering until harvest for early, mid and late-opening terminal (T) ‘Zesy002’ kiwifruit flowers and earlyopening lateral flowers. Flowering time/type

Early T 5% Mid T 50% Late T 95% Lateral1

2015/2016

2016/2017

Flowering date

Harvest time (days after flowering)

Flowering date

Harvest time (days after flowering)

5 November 13 November 20 November 12 November

181 173 166 174

4 November 14 November 21 November 11 November

187 177 170 180

1 Lateral flowers developed only on inflorescences with early terminal flowers.

of each of the four flowering times/types on each of the six vines. Each shoot carried two flowers of the same flowering time/type. 2.3. Shoot manipulation and measurement At flowering each shoot was thinned to leave either two terminal flowers of the same cohort (early, mid and late) or two early-opening lateral flowers from separate inflorescences in the middle of the flowering zone on each shoot. All shoots had 10 ± 1 leaves, were 451 ± 23 mm in length, with 1850 ± 110 cm2 of leaf area and two flowers on separate inflorescences at flowering. Shoots were maintained at this size throughout the experiment to optimise fruit carbohydrate supply. The basal diameter of all shoots and the diameter of the cane on the rootward side of the shoot were measured with digital vernier callipers (Mitutoyo model 500 171 20, Tokyo, Japan) immediately after fruit harvest. In the 2016/2017 season the ovaries were removed from two terminal flowers on each of six additional shoots from each terminal flowering cohort (early, mid and late) when flowers opened and the weight of the ovaries recorded.

2. Materials and methods 2.4. Fruit measurements 2.1. Plant material All fruit were harvested from shoots at commercial harvest on 4 May 2016 or 10 May 2017 (the number of days of fruit development for each flowering time/type are shown in Table 1). At harvest, individual fruit weights were recorded for both fruit on all shoots. Both fruit from two shoots per vine were then measured (see below), while fruit from the remaining two shoots per vine were stored at 1 °C for 8 weeks, ripened at 20 °C for one week and then measured. Fruit external dimensions (length (L), maximum equatorial diameter (D1) and minimum equatorial diameter (D2)) were measured with digital vernier callipers. Fruit shape was calculated from the fruit equatorial diameters and length: (D2/D1 × 100 and L/D2) (CruzCastillo et al., 2002). Fruit firmness was measured with a Fruit Texture Analyser (GUSS model GS14, Cape Town, South Africa) with a 7.9-mm diameter Effegi™ penetrometer probe after a 1-mm thick slice of skin and outer pericarp was removed from adjacent sides of the equatorial region of the fruit (Burdon et al., 2017). The outer pericarp colour intensity was measured with a Minolta CR-300 chromameter (Osaka, Japan) after a 2-mm thick slice of skin and outer pericarp was removed from the equatorial region of the opposite sides of the fruit from firmness measurements (Montefiori et al., 2005). The fruit were cut at the equator and measurements of the maximum and minimum diameters of the core and the inner pericarp were made. These measurements, together with the maximum and minimum diameters of the fruit, were used to calculate the areas of core, inner and outer pericarp in an equatorial plane of the fruit, assuming the fruit shape was an ellipse. The percentage of each tissue type was then determined using the total equatorial cross-sectional area of each fruit. In

Four-year-old Actinidia chinensis var. chinensis ‘Zesy002’ vines grafted on mature Actinidia chinensis (Planch.) var. deliciosa ‘Bruno’ seedling rootstock and located on an orchard in Kerikeri, New Zealand (35°10′S 173°55′E) were used in the study. Six vines were used, spaced 4.5 m apart between the rows and 4.4 m within the row and trained on a horizontal pergola system. Vines were managed using standard practices (Sale and Lyford, 1990) including winter cane pruning and summer pruning to maintain both an open canopy and experimental shoots at a standard size (leaf:fruit ratio of 5:1). Pollination was carried out by honey bees with six hives per ha. 2.2. Experimental design The effects of time of flowering and flower type were evaluated to understand effects on variability in fruit characteristics within vines over two New Zealand growing seasons (2015/2016 and 2016/2017). Time of flower opening was classified for terminal flowers in an inflorescence as early (5% of flowers open), mid (50% of flowers open) or late (95% of flowers open) and the calendar dates are shown in Table 1. The development of lateral flowers on an inflorescence was also compared with that of the terminal flowers; however, lateral flowers developed only on shoots that had early-opening terminal flowers, as lateral flowers aborted before flowering on mid and late flowering shoots. For early-opening lateral flowers, flowers opened 7 days later than terminal flowers on equivalent early flowering shoots (Table 1). The experiment was carried out as a randomised block with four shoots 742

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However in the following season, canes adjacent to shoots that produced either early-opening terminal flowers or lateral flowers both had significantly (P < 0.001) smaller basal diameters than those that produced mid- and late-opening terminal flowers. There was no significant effect of time of flowering on shoot basal diameter in the 2015/ 2016 season. However in the 2016/2017 season, shoots that carried early-opening terminal flowers or lateral flowers had significantly (P < 0.01) smaller diameters than those that carried fruit from midand late-opening terminal flowers. The basal diameters of one-year-old canes, adjacent to shoots that produced flowers, were generally larger in the 2015/2016 growing season than in the 2016/2017 season.

the 2016/2017 season an image was also taken of the equatorial crosssection of each fruit to determine the carpel number. Dry matter content was calculated from a 2-mm thick longitudinal slice removed from the centre of the fruit, containing all tissue types, using the fresh slice weight and dry slice weight after drying at 65 °C for 24 h. An average soluble solids content (SSC) was calculated from measurements of juice squeezed from a 10-mm slice from both the stylar and stem end of the fruit using a hand-held refractometer (0–20%, Atago, Tokyo, Japan), as SSC values at each end of the fruit differ (Hopkirk et al., 1986). Sixteen additional fruit from similar shoots were harvested from the same vines at fortnightly intervals prior to and after harvest to calculate rates of change in fruit characteristics over this time. Growth and maturity rates calculated from these data are shown in supplementary data (Supplementary Table S1) and used with the difference in the fruit development period and harvest data to normalise fruit development to 181 days in 2015/2016 and 187 days in 2016/2017.

3.2. The effect of flowering time and flower type on the weight and dry matter content of fruit at harvest At harvest, the mean weight of fruit that developed from earlyopening terminal flowers was significantly greater (P < 0.001; 12.1 g more in 2015/2016 and 13.2 g in 2016/2017) than that of fruit that developed from late-opening terminal flowers (Fig. 1). The weight of fruit produced from early-opening terminal flowers was not significantly different from that of those fruit that developed from midopening terminal flowers in the 2015/2016 season. However fruit from early-opening terminal flowers weighed significantly (P < 0.001; mean 19.5 g) more than those from mid-opening terminal flowers in the 2016/2017 season. Fruit that developed from mid-opening terminal flowers were significantly (P < 0.001) heavier than those that developed from late-opening terminal flowers in the 2015/2016 season but not in the 2016/2017 season. In both seasons, fruit that developed from the lateral flowers weighed significantly less (P < 0.001; range 10.5–33.5 g) than fruit that developed from terminal flowers, regardless of time of flower opening for terminal flowers. These differences in fruit weight were not affected by the variable lengths of fruit development periods as normalising fruit weight to the longest period of fruit development in each season had no effect (Supplementary Table S1). In the second season, the weight of ovaries from terminal flowers reflected the trends in fruit weight at harvest, whereby the ovaries from early-opening terminal flowers were significantly (P < 0.05) heavier than those from mid- and late-opening terminal flowers (Fig. 2). However, the number of carpels present in fruit that developed from terminal flowers was similar regardless of time of flowering, but the number of carpels present in fruit from lateral flowers was significantly (P < 0.001) less than that in fruit from terminal flowers (Fig. 2). Fruit that developed from lateral flowers also had a significantly (P < 0.001 2015/2016; P < 0.05 2016/2017) higher minimum/maximum diameter ratio than those that developed from terminal flowers, regardless of flower opening time. However, there were no effects of flower opening time or flower type on the length/maximum diameter ratio of fruit (Table 3).

2.5. Fourier transform infrared (FTIR) spectroscopy estimates of SSC, sugar and acidity concentrations A sample of juice was collected from each ripe fruit (< 1 kgf) in the 2016/2017 season for FTIR measurements. Five drops of juice from each of the stylar and stem ends of the fruit were combined and immediately frozen at −20 °C. Tubes were thawed and centrifuged (3 min; 12,000 g) to remove any solids from the sample. Measurement of the FTIR spectrum was carried out using a Bruker Alpha spectrometer (Bruker Corporation, Billerica, MA, USA) as described by Clark (2016). Estimates of SSC, titratable acidity and concentrations of soluble sugars (glucose, fructose and sucrose) and organic acids (malate, quinate and citrate) were calculated using the spectral data and regression model for ‘Zesy002′ fruit (Seal et al., 2017). 2.6. Statistical analysis All data were analysed using the ANOVA technique with GenStat 14th edition for Windows (VSN International Ltd, Hemel Hempstead, Hertfordshire, United Kingdom) and a randomised block design. Comparisons between mean values were made at the appropriate level of significance and P-values are given in the text. 3. Results 3.1. The relationship between flowering time and type, and cane and shoot measurements at harvest At fruit harvest in the 2015/2016 season, the basal diameters of canes adjacent to shoots that carried only lateral flowers were significantly (P < 0.001) less than those of canes adjacent to shoots that carried only terminal flowers across all flower opening times (Table 2).

3.3. The effect of flowering time and flower type on the dry matter content of fruit at harvest

Table 2 The effect of time of flowering (early, mid, late) for terminal (T) ‘Zesy002’ kiwifruit flowers and flower type (terminal (T) or lateral) and one-year-old cane or shoot diameters measured at harvest over two experimental seasons (2015/ 16 and 2016/17). Data are means ± SEM, n = 24. Flowering time/ type

Early T Mid T Late T Lateral Significance1 1

One-year-old cane diameter (mm)

Shoot diameter (mm)

2015/16

2016/17

2015/16

2016/17

17.7 19.1 18.7 15.9 ***

11.4 14.1 15.2 11.8 ***

11.3 11.3 11.4 11.3 ns

11.7 12.0 12.8 11.5 **

± ± ± ±

0.5 0.4 0.5 0.5

± ± ± ±

0.3 0.4 0.3 0.4

± ± ± ±

0.3 0.3 0.3 0.5

± ± ± ±

The dry matter contents of the fruit from early-opening terminal flowers and lateral flowers were significantly (P < 0.001) greater than those of fruit from late-opening terminal flowers in both seasons (Fig. 1). However, the dry matter content of fruit that developed from mid-opening terminal flowers was only significantly (P < 0.001) greater than that of fruit from late-opening terminal flowers in the 2015/2016 season when the weight of fruit from these two flowering cohorts were similar.

0.2 0.3 0.3 0.3

3.4. Tissue proportions The equatorial cross sectional area and the percentage of each tissue type in fruit varied with flowering time and type within each season as well as between the two seasons (Table 4). There was significantly

** P < 0.01, *** P < 0.001, ns not significant. 743

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Fig. 1. The effect of time of flowering (early, mid, late) of terminal ‘Zesy002’ kiwifruit flowers and flower type (terminal (T) or lateral) on mean fruit fresh weight (A and B) and dry matter content (C and D) at harvest in the 2015/2016 and 2016/2017 seasons. Data are means ± SEM, n = 24 for fruit weight, n = 12 for fruit dry matter content.

Table 3 The effect of time of flowering (early, mid, late) for terminal ‘Zesy002’ kiwifruit flowers and flower type (terminal (T) or lateral) on subsequent fruit shape determined by the relationship between the ratios of minimum/maximum fruit diameter and fruit length/minimum fruit diameter at harvest in the 2015/2016 and 2016/2017 growing seasons. Data are means ± SEM, n = 12. Flowering time/type

Early T Mid T Late T Lateral Significance1 1

Minimum/maximum diameter ratio (%)

Length/minimum diameter ratio (%)

2015/16

2016/17

2015/16

2016/17

93.2 91.4 91.3 98.1 ***

92.0 93.1 92.7 95.2 *

66.5 66.6 66.1 70.1 ns

68.4 69.1 68.1 70.5 ns

± ± ± ±

0.8 0.8 0.8 0.8

± ± ± ±

0.7 0.7 0.7 0.7

± ± ± ±

0.7 0.7 0.7 0.7

± ± ± ±

0.5 0.5 0.5 0.4

* P < 0.05, *** P < 0.001, ns not significant.

3.5. Fruit maturity Fig. 2. A. The effect of time of flowering (early, mid, late) on mean ovary fresh weight of terminal ‘Zesy002’ kiwifruit flowers at flowering in 2016/2017. Data are means ± SEM, n = 6. B. The effect of time of flowering (early, mid, late) of terminal flowers and flower type (terminal (T) or lateral) on carpel number per fruit measured at harvest in the 2016/2017 season. Data are means ± SEM, n = 12.

Fruit that developed from early-opening terminal flowers or lateral flowers were significantly (P < 0.01 – 0.001) more mature at harvest (higher SSC, lower firmness and yellow flesh colour) than fruit produced by mid- and late-opening terminal flowers (Table 5). However, when the data were adjusted to the maximum length of fruit development using the rates of fruit maturation near harvest (Supplementary Table S1), the maturity of all fruit, except those of fruit that developed from late-opening terminal flowers in the 2016/2017 season, were similar. The delay in maturation of fruit from late-opening terminal flowers in the 2016/2017 season may be associated with their much lower dry matter content than other fruit in that season.

(P < 0.001) more outer pericarp (8% in 2015/2016, 3% in 2016/ 2017) and less inner pericarp tissue (5% in 2015/2016, 3% in 2016/ 2017) in fruit from early- and mid-opening terminal flowers and lateral flowers than in fruit from late-opening terminal flowers (Table 4). The core tissue made up between 2 and 3% of the equatorial cross-sectional area of the fruit in both seasons but there was no effect of the time of flowering on the percentage of core tissue in fruit that developed from terminal flowers (Table 4). Differences between fruit tissue percentages in the two seasons were large, with more inner pericarp (12%) and less outer pericarp (13%) tissue in all fruit in the 2015/2016 season than in fruit in the 2016/2017 season.

3.6. Fruit juice composition In the 2016/2017 season, SSC concentrations (estimated by FTIR) in the juice of eating-ripe fruit (< 1 kgf firmness) reflected the dry matter content of fruit at harvest. Fruit that developed from late-opening terminal flowers had significantly (P < 0.001) lower SSC than fruit that developed from all other flowering times/types (Table 6). The 744

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Table 4 The effect of flowering time (early, mid, late) of terminal ‘Zesy002’ kiwifruit flowers and flower type (terminal (T) or lateral) on the total area and percentage of each tissue (outer pericarp, inner pericarp and core) in the equatorial cross-section of fruit at harvest in the 2015/2016 and 2016/2017 seasons. Data are means ± SEM, n = 12. Flowering time/type

Early T Mid T Late T Lateral Significance1 1

Total cross sectional area (mm2)

Core (mm2)

2015/16

2015/16 2.5 2.7 2.2 3.0 **

2374 2356 2149 2099 ***

± ± ± ±

2016/17 56 56 56 56

2628 2443 2497 2255 ***

± ± ± ±

42 46 42 42

± ± ± ±

0.2 0.2 0.2 0.2

Inner pericarp (mm2)

Outer pericarp (mm2)

2016/17

2015/16

2016/17

2015/16

2016/17

2.5 2.0 2.1 1.8 ***

29.6 33.1 38.4 30.0 ***

19.5 20.7 22.7 19.7 ns

68.0 64.3 58.6 67.7 ***

78.0 77.4 75.1 78.5 ***

± ± ± ±

0.2 0.2 0.2 0.2

± ± ± ±

1.1 1.1 1.1 1.1

± ± ± ±

0.4 0.4 0.4 0.4

± ± ± ±

1.2 1.2 1.2 1.2

± ± ± ±

0.4 0.4 0.4 0.4

** P < 0.01, *** P < 0.001, ns not significant.

late-opening flowers. These effects were associated with differences in ovary weight and subsequently with differences in the proportion of inner and outer pericarp tissue within the fruit. Although lateral flowers produced smaller fruit than terminal flowers, the tissue proportions, maturity and sugar and acid composition of fruit from lateral flowers reflected those of early-opening terminal flowers that developed on equivalent inflorescences. These results suggest that competition for carbohydrate during flower development can have an important effect on variation in fruit characteristics at harvest, confirming our hypothesis.

difference in SSC was associated with significantly (P < 0.001) lower FTIR estimates of glucose and sucrose concentrations in the juice of fruit that developed from late-opening terminal flowers compared with the juice of fruit that developed from other flowering times/types. Fruit that developed from early-opening terminal or lateral flowers had significantly (P < 0.05 - 0.01) higher FTIR estimates of sucrose but significantly (P < 0.05 - 0.001) lower estimates of fructose concentrations in their juice than fruit that developed on mid- or late-opening terminal flowers. The fructose:glucose ratio in the juice of fruit from late-opening terminal flowers (1.01 ± 0.12), was significantly (P > 0.001) higher than the ratios in the juice of fruit from other flowering times/types (0.85-0.91 ± 0.12). Fruit from late-opening flowers also had a much higher hexose: sucrose ratio (5.07 ± 0.21), significantly (P > 0.001) higher than that of fruit from early-opening terminal (2.20 ± 0.21), mid-opening terminal (3.08 ± 0.22) and lateral flowers (2.51 ± 0.21). In the 2016/2017 season fruit that developed from late-opening terminal flowers had significantly (P < 0.001) higher FTIR-estimated titratable acidity concentrations in their juice than fruit that developed from other flower types (Table 6). There were significantly (P < 0.01 0.001) higher FTIR-estimated quinate and citrate acid concentrations in the juice of fruit from late-opening terminal flowers than in the juice of fruit from other flowering times/types. The FTIR-estimated titratable acidity in the juice of fruit from lateral flowers was also significantly (P < 0.001) lower than that of fruit from mid-opening flowers, associated with lower estimated concentrations of quinate and citrate in fruit (P < 0.05 – 0.01).

4.1. Cane diameter affects flowering time Shoots that produced early-opening terminal or lateral flowers and subsequently fruit with high dry matter and a balanced sugar and acid composition, developed on smaller diameter one-year-old canes than shoots that produced mid- and late-opening terminal flowers. In a recent study of a red Actinidia chinensis genotype, fruit produced on shoots from thinner one-year-old canes also had higher dry matter content than those produced on thicker one-year-old canes and this was attributed to less competition from vegetative growth on the smaller canes (Nardozza et al., 2015). In the current study flowers were selected on similar long shoots with a leaf:fruit ratio of 5:1 but in the second season early-opening terminal and lateral flowers developed on smaller diameter shoots than late-opening flowers. In a study of ‘Hayward’ kiwifruit vines, early-opening flowers, which subsequently produced larger fruit, were found on long non-terminated shoots (leaf:fruit ratio of approximately 5:1) compared with fruit from late-opening flowers that developed on shoots with a leaf:fruit ratios of 2:1. (Lai et al., 1990). This evidence suggests that competition for carbohydrate supply between vegetative and floral growth during spring may influence flowering time and subsequent fruit development.

4. Discussion The aim of this study was to determine whether time of flowering and flower type affect final fruit weight, tissue composition, fruit maturation, and sugar and acid composition of ‘Zesy002’ kiwifruit. The potential fruit weight, fruit tissue proportions, and ripe fruit juice sugar and acid composition of ‘Zesy002’ fruit were determined prior to flowering. Early-opening terminal flowers produced larger, higher dry matter content fruit with a more favourable sugar to acid ratio than

4.2. Fruit weight is related to flowering time and flower type Early-opening terminal ‘Zesy002’ flowers produced larger ovaries and this was correlated with consistently larger fruit than those

Table 5 The effect of time of flowering (early, mid or late) for terminal ‘Zesy002’ kiwifruit flowers and flower type (terminal (T) or lateral) on fruit maturity characteristics (soluble solids content (SSC), firmness and flesh colour) at harvest. Measurements were made on ripe fruit (< 1 kgf) at the end of the 2015/2016 and 2016/2017 seasons. Data are means ± SEM, n = 12. Flowering time/type

Early T Mid T Late T Lateral Significance1 1

SSC (%)

Firmness (kgf)

Flesh colour (hue angle)

2015/16

2016/17

2015/16

2016/17

2015/16

2016/17

15.5 13.7 12.9 15.6 ***

16.1 14.7 11.4 16.2 ***

4.00 5.99 6.17 4.66 ***

3.34 4.79 7.39 3.08 **

97.8 98.3 98.1 96.8 ***

96.2 96.7 98.0 96.4 **

± ± ± ±

0.4 0.4 0.4 0.4

± ± ± ±

0.3 0.3 0.3 0.3

** P < 0.01, *** P < 0.001. 745

± ± ± ±

0.24 0.24 0.24 0.24

± ± ± ±

0.30 0.32 0.30 0.30

± ± ± ±

0.2 0.2 0.2 0.2

± ± ± ±

0.2 0.2 0.2 0.2

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Table 6 : The effect of time of flowering (early, mid or late) for terminal ‘Zesy002’ kiwifruit flowers and flower type (terminal (T) or lateral) on Fourier Transform Infrared spectroscopy estimates of soluble solids content (SSC), individual sugar concentrations, titratable acidity and individual acid concentrations in the juice of eating-ripe fruit. Fruit were harvested in the 2016/2017 season and stored for 8 weeks at 1 °C and 1 week at 20 °C. Data are means ± SEM, n = 12. Flowering time/type

SSC (%)

Titratable acidity (%)

Juice concentration (mg/100 mL juice) Glucose

Early T Mid T Late T Lateral Significance1 1

19.8 19.3 17.4 19.6 ***

± ± ± ±

0.3 0.3 0.3 0.3

0.508 0.616 0.897 0.415 ***

± ± ± ±

0.039 0.041 0.039 0.039

6688 6746 5978 6994 ***

± ± ± ±

Fructose 92 95 92 92

5772 6150 6024 5974 ***

± ± ± ±

Sucrose 60 62 60 60

6124 4821 2655 5726 ***

± ± ± ±

Malate 291 301 291 291

194 204 236 184 *

± ± ± ±

13 13 13 13

Quinate

Citrate

350 403 588 307 ***

554 617 753 459 ***

± ± ± ±

25 26 25 25

± ± ± ±

29 30 29 29

* P < 0.05, *** P < 0.001.

produced by late-opening terminal flowers. This is consistent with previous studies of kiwifruit where early-opening ‘Hayward’ kiwifruit flowers had larger ovaries and produced larger fruit at harvest (Lai et al., 1990), early-opening terminal flowers of a red Actinidia chinensis genotype produced larger fruit (Nardozza et al., 2015) and flowers treated with the cytokinin-like compound forchlorfenuron (CPPU) before anthesis produced larger fruit (Cruz-Castillo et al., 2014). However, ovary weight was not correlated with the final fruit weight in a study of ‘Hayward’ kiwifruit across several sites and over two seasons by McPherson et al. (2001b), possibly because of environmental effects or sampling across a range of shoot types in that study. Ovary weight was correlated with final fruit weight at harvest in olive (Rosati et al., 2009), grape (Gray and Coombe, 2009) apple (Denne, 1963), citrus (Guardiola et al., 1984; Guardiola and Lazaro, 1987) and peach (Scorza et al., 1991). The relationship between ovary and subsequent fruit weight appeared to be related to carbohydrate supply through spur size in apple (Denne, 1963), and leafiness of the inflorescences and crop load in citrus (Guardiola et al., 1984; Guardiola and Lazaro, 1987). In kiwifruit, flower differentiation competes with early shoot growth before shoots become autotrophic (Greer and Jeffares, 1998) and it is likely that early-opening flowers are more competitive than later-opening flowers for the limited amounts of reserve carbohydrate available. Kiwifruit inflorescences generally have a terminal flower and two lateral flowers; however, the lateral flowers often abort before opening (Hopping, 1990). In the current study lateral flowers only developed fully on ‘Zesy002’ shoots with early-opening terminal flowers. In a previous study of ‘Hayward’ kiwifruit by Antognozzi et al. (1991) lateral flowers produced significantly smaller fruit regardless of the number of flowers retained on the inflorescence and this difference was explained by lateral flowers having less vascular tissue than the terminal flower. In pomegranate inflorescences terminal flowers were also larger than lateral flowers (Wetzsteini et al., 2013), and asynchronous cell division within the floral primordium of highly branched grape inflorescences (Gray and Coombe, 2009) caused variation in berry weight (Friend et al., 2009). In kiwifruit inflorescences the development of lateral flowers lags behind that of terminal flowers (Richardson et al., 2001), resulting in smaller ovaries and hence smaller fruit developing from lateral flowers than from terminal flowers and hence lateral flowers are generally removed during thinning.

produced fruit with lower SSC at harvest than fruit from later-opening flowers (Fukuda et al., 2015). This difference may be because peach flowers differentiate before the end of winter dormancy and open in early spring (Reinoso et al., 2002) when temperatures are low, while kiwifruit flowers differentiate during an extended period in spring in competition with shoot growth (Brundell, 1975). In the current study lateral flowers produced fruit with a similar dry matter content to those that developed from early-opening terminal flowers on equivalent shoots. This is consistent with the findings of a previous study of ‘Hayward’ kiwifruit by Antognozzi et al. (1996), where lateral fruit had similar dry matter contents to terminal fruit regardless of whether the inflorescence carried a terminal and two lateral fruit or either a single terminal or single lateral fruit. This suggests that the fruit’s ability to accumulate dry matter is a feature of the inflorescence and its time of development, rather than of flowering type per se. Kiwifruit, like tomato, contain several distinct tissue types in their fruit whereas in apples, peaches and grapes much of the fruit tissue is homogeneous. In the current study, ‘Zesy002’ fruit that developed from late-opening terminal flowers had a higher percentage of inner pericarp tissue and less outer pericarp tissue than those that developed from early-opening terminal flowers. In a previous study, fruit that developed from early-opening ‘Hayward’ flowers had more core cells than fruit from late-opening flowers, but the number and size of inner and outer pericarp cells were similar (Cruz-Castillo et al., 2002). However, Nardozza et al. (2011) found that although the tissue proportions did not vary between Actinidia chinensis var. deliciosa genotypes with differing fruit dry matter contents, the number of small high starch-containing cells in the outer pericarp was greater in the fruit of high dry matter genotypes than in the low dry matter genotypes. Previous studies of ‘Hayward’ kiwifruit have shown that applications of the cytokinin-like compound forchlorfenuron (CPPU) generally increase fruit weight and decrease fruit dry matter content (Patterson et al., 1993; Antognozzi et al., 1996; Nardozza et al., 2017). This effect of CPPU has been associated with increased cell size (Woolley et al., 1991; Patterson et al., 1993; Antognozzi et al., 1997) or increased cell number (Antognozzi et al., 1997; Cruz-Castillo et al., 2002), particularly in the outer pericarp, as well as changes in the starch and hexose metabolism (Antognozzi et al., 1996; Nardozza et al., 2017) in the fruit. Therefore the relationship between the proportions of pericarp tissue in fruit, cell types in the outer pericarp and composition of fruit from different flower types warrants further investigation.

4.3. Late-opening terminal flowers produce fruit with lower dry matter and less outer pericarp tissue

4.4. Fruit maturity and time of harvest

Late-opening terminal flowers produced fruit that had consistently lower dry matter contents than fruit that developed from early-opening terminal flowers. There are few other studies on the time of flowering and its subsequent effect on fruit quality; however, in a red Actinidia chinensis genotype late-opening terminal flowers also produced fruit with a lower dry matter content than early-opening terminal flowers (Nardozza et al., 2015). In contrast, early-opening peach flowers

In this study fruit were harvested on a single date, as would typically occur in a commercial orchard. Despite the fact that fruit were quite mature at harvest (mean SSC 14.4%), there were still significant differences in the composition (SSC, firmness and flesh colour) of the fruit from early-opening terminal and lateral flowers compared with fruit that developed from mid- or late-opening terminal flowers. Generally this was due to the differences in the duration of fruit 746

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development, caused by the variation in flowering dates. A similar relationship between time of flowering and SSC accumulation has been shown in grape berries (Coombe, 1980; May, 1987; Trought et al., 2017). However, fruit that developed from late-opening terminal flowers in 2016/2017 were still less mature at harvest than fruit from other flowering time/types after the period of fruit development had been normalised. These fruit had a dry matter content two units lower than fruit from other flower times/types. Different fruit maturity patterns have also been shown in low dry matter ‘Hort16A’ kiwifruit (Boyd and Barnett, 2011) and also in the fruit of apple, citrus, grape and peach (Allan et al., 1993; Palmer et al., 1997; Keller et al., 2008; PoirouxGonord et al., 2012; Parker et al., 2015). Results from the current study and a previous study of ‘Hayward’ fruit (Antognozzi et al., 1991) showed that there were no differences in the maturity of fruit that developed from early-opening terminal and lateral flowers from equivalent inflorescences despite a seven-day difference in the time of flower opening. The current study suggests that considerable variation in fruit composition can occur because of the spread of flowering date, and may affect postharvest performance and consumer acceptance of fruit.

This work was part of the New Zealand Institute for Plant and Food Research Limited Premium Kiwifruit Programme funded through the New Zealand Ministry of Business, Innovation and Employment Strategic Science Investment Fund. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.scienta.2018.11.043. References Allan, P., George, A.P., Nissen, R.J., Rasmussen, T.S., 1993. Effects of girdling time on growth, yield, and fruit maturity of low chill peach cultivar Flordaprince. Aust. J. Exp. Agric. 33, 781–785. https://doi.org/10.1071/ea9930781. Antognozzi, E., Battistelli, A., Famiani, F., Moscatello, S., Stanica, F., Tombesi, A., 1996. Influence of CPPU on carbohydrate accumulation and metabolism in fruits of Actinidia deliciosa (A Chev.). Sci. Hortic. 65, 37–47. https://doi.org/10.1016/03044238(95)00852-7. Antognozzi, E., Famiani, F., Proietti, P., Tombesi, A., Ferranti, F., Frenguelli, G., 1997. Effect of CPPU (cytokinin) treatments on fruit anatomical structure and quality in Actinidia deliciosa. Acta Hortic. 1 & 2, 459–465. Antognozzi, E., Tombesi, A., Ferranti, F., Frenguelli, G., 1991. Influence of sink competition on peduncle histogenesis in kiwifruit. N. Z. J. Crop Hortic. Sci. 19, 433–439. https://doi.org/10.1080/01140671.1991.10422889. Boyd, L.M., Barnett, A.M., 2011. Manipulation of whole-vine carbon allocation using girdling, pruning, and fruit thinning affects fruit numbers and quality in kiwifruit. HortScience 46, 590–595. Boyd, L.M., Ramankutty, P., Barnett, A.M., Dawson, T., Wegrzyn, T., Le Guevel, A., Mowat, A.D., 2008. Effect of canopy position on fruit quality in’ Hort16A’ kiwifruit in New Zealand. J. Horticult. Sci. Biotechnol. 83, 791–797. https://doi.org/10.1080/ 14620316.2008.11512462. Brundell, D.J., 1975. Flower development of the chinese gooseberry (Actinidia chinensis Planch.) II. Development of the flower bud. N. Z. J. Bot. 13, 485–496. Burdon, J., Pidakala, P., Martin, P., Billing, D., 2017. Softening of’ Hayward’ kiwifruit on the vine and in storage: the effects of temperature. Sci. Hortic. 220, 176–182. https:// doi.org/10.1016/j.scienta.2017.04.004. Clark, C.J., 2016. Fast determination by Fourier-transform infrared spectroscopy of sugaracid composition of citrus juices for determination of industry maturity standards. N. Z. J. Crop Hortic. Sci. 44, 69–82. https://doi.org/10.1080/01140671.2015.1131725. Coombe, B.G., 1980. Development of the grape berry. I. Effects of timing of flowering and competition. Aust. J. Agric. Res. 31, 125–131. https://doi.org/10.1071/ar9800125. Crisosto, C.H., Crisosto, G.M., 2001. Understanding consumer acceptance of early harvested’ Hayward’ kiwifruit. Postharvest Biol. Technol. 22, 205–213. https://doi.org/ 10.1016/s0925-5214(01)00097-7. Cruz-Castillo, J.G., Baldicchi, A., Frioni, T., Marocchi, F., Moscatello, S., Proietti, S., Battistelli, A., Famiani, F., 2014. Pre-anthesis CPPU low dosage application increases’ Hayward’ kiwifruit weight without affecting the other qualitative and nutritional characteristics. Food Chem. 158, 224–228. https://doi.org/10.1016/j.foodchem. 2014.01.131. Cruz-Castillo, J.G., Woolley, D.J., Lawes, G.S., 2002. Kiwifruit size and CPPU response are influenced by the time of anthesis. Sci. Hortic. 95, 23–30. https://doi.org/10.1016/ s0304-4238(01)00384-3. Denne, P.M., 1963. Fruit development and some tree factors affecting it. N. Z. J. Bot. 1, 265–294. Ferguson, A.R., 2015. Kiwifruit in the World-2014. Acta Hortic. 1096, 33–46. Friend, A.P., Trought, M.C.T., Creasy, G.L., 2009. The influence of seed weight on the devlopment and growth of berries and live green ovaries in Vitis vinifera L. Pinot Noir and Cabernet Sauvignon. Auts. J. Grape Wine Res. 15, 166–174. https://doi.org/10. 1111/j.1755-0238.2009.00050.x. Fukuda, F., Hirano, K., Morinaga, K., Kubota, N., 2015. Flower and fruit thinning in relation to some fruit traits as affected by bloom time and within-tree position in peach. Acta Hortic. 1084, 495–502. Gray, J.D., Coombe, B.G., 2009. Variation in Shiraz berry size originates before fruitset but harvest is a point of resynchronisation for berry development after flowering. Auts. J. Grape Wine Res. 15, 156–165. https://doi.org/10.1111/j.1755-0238.2009. 00047.x. Greer, D.H., Jeffares, D., 1998. Temperature-dependence of carbon acquisition and demand in relation to shoot growth of kiwifruit (Actinidia deliciosa) vines grown in controlled environments. Aust. J. Plant Physiol. 25, 843–850. https://doi.org/10. 1071/pp98055. Guardiola, J.L., Garciamari, F., Agusti, M., 1984. Competition and fruit-set in the Washington navel orange. Physiol. Plant. 62, 297–302. https://doi.org/10.1111/j. 1399-3054.1984.tb04576.x. 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4.5. Sugar acid balance Consumers are sensitive to both sugar and acid concentrations as well as associated changes of flavour volatiles in ripe fruit (Rossiter et al., 2000; Marsh et al., 2006). In the current study late-opening terminal flowers produced fruit with lower estimated glucose and sucrose concentrations and higher quinate and citrate concentrations in their juice than fruit from other flower timings/types, and this is likely to detract from the sensory perception of fruit from late-opening flowers. MacRae et al. (1989) suggested that higher percentages of inner pericarp in ‘Hayward’ fruit may increase the consumers’ perception of low sugar and high acid, as carbohydrate and acid composition varied between fruit tissues during fruit maturation. In the present study of ‘Zesy002’ fruit, a higher percentage of inner pericarp tissue in fruit from late-opening terminal flowers was associated with higher estimated concentrations of citrate and quinate as well as higher fructose:glucose and hexose:sucrose ratios in ripe fruit juice than in the juice of fruit that developed from early-opening terminal or lateral flowers. This suggests that the metabolic pathways may be altered in the fruit tissues, as for example in tomato berries from different cultivars where there is more hexose turnover in locular gel (inner pericarp) than in the outer pericarp tissue (Schouten et al., 2016). In ‘Zesy002’ fruit this change may occur through either starch metabolism (dry matter) (Nardozza et al., 2011) or the sugar and acid metabolism in different tissues and cells (Nardozza et al., 2017). 5. Conclusion The results from this study suggest that both the date of flower opening and flower type (terminal vs lateral) of ‘Zesy002’ kiwifruit are related to variation in final fruit weight and fruit composition at harvest. The association between fruit composition and fruit tissue proportions suggests that the proportions of inner and outer pericarp tissue or cell types within these tissues affect fruit sink strength and sugar:acid balance. Differences in tissue proportions within ‘Zesy002’ appear to be determined before flowering and this may be related to competition between vegetative and reproductive sinks for carbohydrate supply during flower differentiation in spring. Acknowledgements We thank Dr Marc Greven and Dr Jem Burdon for critical reading of the manuscript, and Dr Simona Nardozza and Dr Chris Clark for helpful suggestions. We also acknowledge the staff of the Kerikeri Research Centre for assistance with measurements and maintenance of plants. 747

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