Internal versus external control of calcium nutrition in kiwifruit

Review Article

Internal versus external control of calcium nutrition in kiwifruitGiuseppe Montanaro1*, Bartolomeo Dichio1, Alexander Lang2, Alba N. Mininni1, Vitale Nuzzo1, Michael J. Clearwater3,and Cristos Xiloyannis1

1 Universita degli Studi della Basilicata, Dipartimento delle Culture Europee e del Mediterraneo: Architettura, Ambiente, Patrimoni Culturali,Via S. Rocco, 3 - 75100 Matera, Italy2 Sandy Lang Ltd, 402 Muritai Road, Eastbourne 5013, New Zealand3 Department of Biological Sciences, University of Waikato, Hamilton 3240, New Zealand

Abstract

Higher calcium (Ca) concentration in several fleshy fruit including kiwifruit is a pre-requisite forlower incidence of Ca-related diseases and improved fruit nutritional value. This review exam-ines the internal and external factors operating along the soil-to-fruit pathway that are involved inthe uptake and partitioning of Ca in kiwifruit vines. After a brief description of fruit growth and thedynamic of nutrient accumulation during fruit development, the review considers the role of soilCa concentration and availability, root elongation, mass flow in the apoplast, fruit transpiration,competition between fruit and highly transpiring leaves, weather variables and soil moisture.How fruit morphological and anatomical traits, including skin anatomy, xylem development andhydraulic resistance, influence physiological processes such as transpiration and impact on Caaccumulation is also discussed. The review highlights that approximately 80% of the total Cacontent of fruit is accumulated during the early weeks after fruit-set, suggesting that failure ofgood fruit Ca nutrition at that time may lead to poor fruit Ca content at harvest. Therefore, basedon the analysis of the internal and external factors that influence Ca accumulation, recommenda-tions are made for orchard practices that maximize Ca accumulation in the kiwifruit berry, includ-ing optimal pollination, nutrient and irrigation management, and manipulation of canopy architec-ture.

Key words: Actinidia deliciosa / fruit transpiration / irrigation / mineral elements / soil management /xylem transport

Accepted August 28, 2014

1 Introduction

Calcium (Ca) in plants has both physiological and structuralfunctions. Higher Ca supply is associated with higher yieldsand resistance to some biotic and abiotic stressors (Whiteand Broadley, 2003; Conn and Gilliham, 2010). In addition,optimal Ca concentration of fruit and vegetables at harvestimproves their storability and reduces economic losses be-cause of its role in maintaining tissue mechanical strength(Hirschi, 2004). High Ca concentration is also associated withreductions in the incidence of pre- and post-harvest physio-logical disorders in fruits such as apple, avocado, tomato,grape and kiwifruit (Saure, 1996; Ferguson and Watkins,1989; Cutting and Bower, 1989; Witney et al., 1990; Ho andWhite, 2005; Thorp et al., 2003; Ferguson et al., 2003,Ciccarese et al., 2013).

Plant tissues represent the main dietary source of mineral ele-ments, vitamins, fibers, and other nutrients required for hu-man wellbeing (Stein, 2010; White and Brown, 2010). Currentresearch also suggests that an adequate intake of Ca may re-duce the risk of suffering from chronic diseases such as os-

teoporosis, cancer and hypertension (Martın-Diana et al.,2007). Therefore, increasing the Ca concentration of fruit isconsidered beneficial for both the horticultural industry andthe consumers’ diet.

Edible plant tissues can contain low amounts of certain miner-als for a range of reasons, including low soil (or substrate) nu-trient availability, antagonism between nutrients in the soil, orbecause of limitations in nutrient transport or uptake withinthe plant. In particular, some edible plant organs such asfruits, tubers and seeds may contain low concentrations ofminerals that have restricted phloem mobility. This is particu-larly the case with Ca which is usually classified as mobile inthe xylem only (Bukovac and Wittwer, 1957). As a conse-quence, exogenous Ca applications are often used to en-hance the calcium concentration of fresh fruit and vegetablesin order to extend their shelf life and improve their nutritionalvalue [see Tzoutzoukou and Bouranis (1997) and Martın-Diana et al. (2007) for review; Ciccarese et al., 2013].

At the scale of the whole fruit, the cell wall represents about60–75% of total fruit Ca; the remaining fraction is stored in

ª 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.plant-soil.com

J. Plant Nutr. Soil Sci. 2014, 000, 1–12 DOI: 10.1002/jpln.201400396 1

*Correspondence: Dr. G. Montanaro;e-mail: [email protected]

cellular organelles such as the vacuole, and only a small frac-tion is freely available as active ionic form (Vitagliano et al.,1999; De Freitas and Mitcham, 2012). In this review we referalways to total Ca unless specified otherwise. After a briefpresentation of the growth and seasonal accumulation patternof nutrients in leaves and berries of kiwi (Actinidia deliciosa),we review the current understanding of the physiologicalmechanisms for Ca accumulation in fruit and discuss the de-velopment of environmentally ‘smart’ interventions thatachieve gains in kiwifruit Ca nutrition.

2 Fruit and leaf growth

The growth curve of developing kiwifruit berry fresh weight isdouble-sigmoid and can be divided into three stages (Fig. 1).Stage I (from anthesis to approximately 50 d after fruit set,DAFS), during which fruit grow rapidly, reaching more thanhalf of the final size. The fast initial growth of fruit is attributedto cell division and cell expansion in the pericarp Hopping(1976). The fruit growth rate then slows during Stage II(50–80 DAFS) before accelerating and then slowing graduallyuntil fruit maturity (Stage III, 80–180 DAFS) according to var-iations in the rate of cell enlargement (Hopping, 1976). Incontrast, fruit dry weight gain is relatively constant throughoutthe season (Fig. 1). This reflects the approximately constantrate of whole-fruit phloem import throughout much of fruit de-velopment (Morandi et al., 2010). More recently, a model ofkiwifruit berry development was presented that simulatesgrowth in fresh and dry weight as a function of xylem andphloem inflows and cell-wall extensibility (Hall et al., 2013).Model sensitivity analyses emphasized that growth is sensi-tive to parameters controlling water inputs and demand, par-ticularly early in fruit development when xylem water inflowsare higher. It is during the early phase of fruit development(Stage I) that most of the fruit calcium accumulates, and thefactors that affect water flow in the xylem, growth in freshweight and fruit Ca accumulation are intimately connected.

The typical pattern of sigmoidal leaf area index (LAI; m2 leafarea m–2 soil) development of a kiwifruit canopy is shown in

Fig. 2, along with growth of fruit and shoot (normalized to finaldry weight, DW). Leaf area increases rapidly at first (0–50 dfrom budbreak) with the formation of approximately 70% ofthe maximum LAI. Final maximum leaf area is then reachedat a lower expansion rate approximately 80 d from budbreak.The absolute value of LAI may change according to the train-ing system and the scion/rootstock combination (Smith et al.,1994; Clearwater et al., 2006). In terms of carbon accumula-tion, the current-year leaves and shoots continue to growthroughout the period of fruit development (Fig. 2) suggestingthat competition for assimilates and minerals occurs betweenthese organs at least until the end of Stage II of fruit growth(Figs. 2 and 3).

3 Seasonal leaf and fruit nutrientaccumulation

On a canopy-area basis nutrient uptake is dominated by leafand fruit growth, while nutrient demand by current-seasonstems is relatively low (Fig. 3). Total N, K and Ca are accumu-lated by the kiwifruit canopy to the highest levels (approx.110, 174 and 190 kg ha–1, respectively), whilst total demandfor P and Mg is lower (approx. 8 and 45 kg ha–1, respectively).As expected, the largest difference in nutrient accumulationbetween leaves and fruit is in the phloem-immobile Ca.Leaves account for approximately 85% (Fig. 3) to 93%(Buwalda and Smith, 1987) of total Ca uptake, confirming theweakness of the fruit to acquire Ca because of its low rate oftranspiration compared to the leaves (Xiloyannis et al., 2001).In contrast, the fruits accumulate 50% or more of the morephloem-mobile nutrients N, P and K by the end of the season.

3.1 Fruit calcium and transpiration

As in most fleshy fruit, the Ca concentration in kiwifruit is high-est early after fruit set, thereafter it declines quickly concomi-tant with the beginning of rapid fruit growth (Stage I; Saure,


Frui

t wei

ght /

g

Figure 1: Seasonal pattern of fruit fresh (FW; *) and dry (DW; *)weight (g) of kiwifruit. Each point is the mean of 10 fruits, bars arestandard errors. (Montanaro, unpublished).

Frui

t and

sho

ot g

row

th/ %

of f

inal

DW

shoot

Figure 2: Seasonal pattern of leaf area index (LAI; *) fitted with asigmoidal curve, and fruit (*) and current shoot (leaves and stems)growth (columns) in dry weight relative to final dry weight (%) in a per-gola-trained Hayward kiwifruit orchard (625 plants ha–1). Error barsare SE; the gray filled strips identify stages I, II and III of fruit growth[see Fig. 1; redrawn from Xiloyannis et al. (1999) and Montanaro etal. (2006)].

2 Montanaro, Dichio, Lang, Mininni, Nuzzo, Clearwater, Xiloyannis J. Plant Nutr. Soil Sci. 2014, 000, 1–12

2005; Fig. 4). The dominant reason for decreasing Ca con-centrations is dilution, because fruit size continues to in-crease while Ca import slows due to a number of co-occurringfactors that are described below. In terms of total accumula-tion (i.e., mass per fruit), Ca exhibits an asymptotic-like pat-tern and approaches its maximum at the beginning of Stage IIof fruit growth (at approximately 55 DAFS; Fig. 4). Accordingto earlier reports, around 80% of the Ca present at harvesthad entered the fruit by the end of Stage I, while for others nu-

trients (e.g., K) that percentage is lower, varying between37–55% (Clark and Smith, 1988; Xiloyannis et al., 2001). Dur-ing the remaining weeks until harvest, Ca enters the fruit at avery slow rate, with the last 6 weeks of fruit development re-sulting in a minimal gain in Ca (Fig. 4). In contrast, amounts ofN and K (both highly phloem-mobile) increase linearly for alonger period after full bloom (up to 120 DAFS), with accumu-lation slowing significantly around 140 DAFS (Xiloyannis etal., 2008).


Nitr

ogen

/ kg

ha–1

Phos

phor

us/ k

g ha

–1C

alci

um/ k

g ha

–1

Mag

nesi

um/ k

g ha

–1Po

tass

ium

/ kg

ha–1

Figure 3: Seasonal accumulation (kg ha–1)of (A) nitrogen, (B) magnesium, (C) phos-phorus, (D) potassium and (E) calcium inleaf (*), fruit (*) and 1-year stems (~) of apergola trained Hayward kiwifruit orchard(625 plants ha–1), with a final fruit yield ofapproximately 35 t ha–1.

Cal

cium

con

tent

/ m

g fr

uit–1

Cal

cium

con

cent

ratio

n / %

DW

Tran

spira

tion

/ mm

ol m

–2s–1

Figure 4: Seasonal pattern of Ca accumula-tion (mg fruit–1; &), Ca concentration (%DW; !) and fruit transpiration (* mmol m–2

s–1) in berries of kiwifruit. Data are redrawnfrom Montanaro et al. (2006). Note that thegrey strips represent the fruit growth Stages(see Fig. 1).

J. Plant Nutr. Soil Sci. 2014, 000, 1–12 Calcium nutrition of kiwifruit 3

Calcium moves upward in the plant exclusively in the xylemsap, driven by transpiration and root pressure (Bangerth,1979; Ho et al., 1993; Taylor and Locascio, 2004). Fruit waterloss is highest in young fruit just after fruit set, thereafter it de-clines steeply towards a minimum value at the end of Stage IIof fruit growth where it remains until the end of season(Fig. 4). Figure 5 highlights how well cumulative transpirationpredicts fruit Ca accumulation, illustrating the tight relation-ship between these two processes. Higher transpiration pro-motes higher Ca accumulation in fruit (without any detectableeffect on phloem-mobile K; Fig. 6). However, when a range offruits or environments are compared, there is no simple pro-portionality between them because differences in transpira-tion only partly explain differences in Ca content, particularlywhen transpiration rates are low (Bangerth, 1979).

4 External factors

In the following sections, the external factors (e.g., light inten-sity, wind speed, soil salinity, pH, moisture) involved in fruitCa accumulation are reviewed. Possibilities to develop or-chard practices with the potential to promote an orchard mi-croclimate favorable to fruit Ca nutrition are discussed.

4.1 Radiation

Light is the environmental factor that has the strongest influ-ence on fruit yield and quality of many tree crops, including ki-wifruit (Montanaro et al., 2006, and references therein).Transport of Ca to the fruit preferentially occurs in the apo-plast and xylem vessels, where the rate of transportation de-pends on Ca2+ exchange sorption on the xylem walls, on tran-spiration rate (McLaughlin and Wimmer, 1999; Bangerth,1979; Banuelos et al., 1987) and on xylem functionality of thefruit (Dichio et al., 2003; Mazzeo et al., 2013). Higher lightavailability to fruiting shoots significantly increases final Caconcentration in kiwifruit by approximately 40–80% (Fig. 7).Accumulation of Ca (mass per fruit) remains typically anasymptotic-like curve (see Fig. 5) regardless of the level of ir-radiance. However, increased light availability increases totalfruit Ca content by up to 80% during the first 40 DAFS, withthis enhancement persisting until harvest (Montanaro et al.,2006).

The beneficial effect of higher irradiance on Ca nutrition hasbeen attributed to a light-induced increase in vascular devel-opment within the fruit pedicel and berry (Biasi and Altamura,1996) possibly due to increased concentration of some sec-ondary metabolites involved in the xylogenesis pathway(Montanaro et al., 2007). However, the direct role of light as adriving force for fruit transpiration (see Nobel, 2005) in kiwi-fruit was examined in a modeling exercise and found to benot significant because most of transpiration changes are re-lated to variations of air temperature and relative humidity towhich light is intimately correlated (Montanaro et al., 2012).


Cal

cium

con

tent

/ m

g fr

uit–1

Cum

ulat

ive

tran

spira

tion

/ g H

2O fr

uit–1

(Montanaro et al., 2012)(Clark and Smith, 1988)

Figure 5: Cumulative fruit transpiration (g H2O fruit–1; continuous line;Montanaro et al., 2012) and calcium content (mg fruit–1; Clark andSmith, 1988) in berries of kiwifruit throughout the growth season.

Nut

rient

con

cent

ratio

n / %

DW

Figure 6: Calcium, potassium and magnesium concentrations (%DW) (– SE) measured at harvest in low (L) and high (H)-transpiringberries of kiwifruit and apricot fruit. Comparing treatments within thesame mineral element * indicates a significant difference at P < 5%(Student’s t-test). Redrawn from Xiloyannis et al. (2008) and Monta-naro et al. (2010).

Ca

conc

entr

atio

n / %

DM

Figure 7: Calcium concentration at maturity (% DM – SE, approx.150 DAFS) measured in berries of kiwifruit grown under different irra-diance levels. The shade treatment received approx. 400 mol m–2 s–1

PAR (< 20% available light) at midday.


4.2 Vapor pressure deficit (VPD)

Transpiration of berries of kiwifruit varies in sympathy with thedaily oscillation of environmental parameters (air tempera-ture, humidity, radiation) and is correlated with the vapor pres-sure deficit (VPD; Fig. 8). The role of VPD as the main driverof fruit transpiration was examined recently using a mechanis-tic model (Montanaro et al., 2012). Based on Fick’s first law(Nobel, 2005), specific fruit transpiration rate (E), i.e., the watervapor (wv) efflux per unit area of skin surface, depends on theproduct of the of total fruit conductance to water vapor (gtotal

wv )and the driving ‘‘force’’ (Dwv) causing the vapor diffusion:

E ¼ gtotalwv Dwv (1)

Since total water vapor conductance of the fruit depends onskin conductance (gfruit

wv ) operating in series with the boundarylayer conductance (gbl

wv), fruit transpiration can be extendedas follow:

E ¼ gfruitwv gbl

wv

gfruitwv þ gbl

wvDwv : (2)

The effect of skin properties and wind speed on skin andboundary layer conductance will be examined later. The termDwv is the difference in water vapor pressure between the air-spaces inside the fruit and the air immediately outside it. Thewater vapour pressure within the intercellular airspaces isclose to the saturation value for pure water (Nobel, 2005) atfruit temperature. This means that transpiration will be drivenby the VPD of the bulk atmosphere, assuming fruit tempera-ture is the same as air temperature (Smith et al., 1995).

These conditions mean that Dwv @ VPD, hence Eq. 2 can beexpressed as:

E ¼ gfruitwv gbl

wv

gfruitwv þ gbl

wvVPD: (3)

It follows that fruits growing under higher relative humidity(i.e., low VPD) have a lower transpiration rate (Fig. 8). Accord-ingly, results presented by Li et al. (2002) show that an in-crease in relative humidity from 40 to 60% induced a reduc-tion in fruit water loss by approximately 30–50% in two peachvarieties under laboratory condition. Similarly, for tomato fruita 50–60% reduction in VPD induces a reduction in transpira-tion of approximately 60% (Leonardi et al., 2000).

The relationship presented in Fig. 8 creates the basis for asimple method to estimate fruit transpiration from VPD. How-ever, the proportionality between fruit transpiration and VPD(total conductance, Eq. 2) varies throughout the season, pri-marily because of changes in fruit skin properties. The inclu-sion of skin conductance (gfruit

wv ) and its seasonal variation inthe transpiration model (Eq. 3) improves predictions of tran-spiration rate (R2 up to 0.92) for any given time of day orstage of fruit development (Montanaro et al., 2012).

Based on the mechanism proposed by Montanaro et al.(2012), it is expected that fruit exposed to higher VPD duringgrowth accumulate more Ca because of their higher transpi-ration rate. This effect has been previously documented inapricot, with fruit accumulating 6 and 1.2 mg fruit–1 Ca whengrowing under high and low VPD, respectively (Montanaro etal., 2010). Similarly, fruit of kiwifruit had a Ca concentration atharvest of » 0.17% DW when grown with a low VPD, and» 0.21% DW with a high VPD (P < 5%, Student’s t-test;Montanaro et al., in preparation).

4.3 Wind speed

The transpiration rate of a leaf or fruit is expected to be af-fected by the boundary layer conductance (Eq. 3), which inturn is a function of wind speed (Nobel, 2005). A laboratoryexperiment confirmed this effect for kiwifruit, showing that arti-ficially increasing wind speed up to 3 m s–1 induced higher


Frui

t tra

nspi

ratio

n

Figure 8: Relationship between (normalized) vapor pressure deficit(VPD) and (normalized) transpiration of berries of kiwifruit. Each pointis the mean of 6 fruits measured hourly (approx. 0–24 h) at 23, 35,49, 65, 94, and 140 d after full bloom. Original data (Montanaro et al.,2012) ranged from 0.026 to 0.981 mmol cm–2 h–1 (transpiration) andfrom 0.29 to 4.2 kPa (VPD) due to daily and seasonal oscillations;hence, the data were scaled [min–max normalization, (0,1) range]before plotting.

Net

incr

ease

in fr

uit w

ater

loss

/ mg

cm–2

min

–1

Windspeed / m s–1

Figure 9: Net increase in fruit water loss (mg cm–2 min–1) measuredin detached kiwifruit after wind speed was changed from 0 to 2 m s–1.In the inset: fruit-transpiration response to a range of wind speedsmeasured in young (13 DAFS, *) and old (119 DAFS, *) fruits.Each point is the average of six fruits (– SE). Adapted from Mazzeoet al. (2011).


water loss from detached kiwifruit berries (see inset of Fig. 9).The response of fruit transpiration to wind speed was affectedby fruit age, with no response in fruits older than approxi-mately 50 days (Fig. 9; Mazzeo et al., 2011). Dichio et al.(2003) further corroborated the beneficial effect of high windspeed on Ca accumulation.

Hence, the transpiration equation (Eq. 3) including the influ-ence of boundary layer conductance (in series with skin con-ductance) is applicable to young fruit. However, for typical or-chard wind speeds (< 1.5–2.0 m s–1), fruit boundary layerconductance is high compared to skin conductance, and thefruit transpiration rate is therefore determined primarily byskin conductance even in young fruit (Nobel, 1975; Dichio etal., 2003). This in turn renders the boundary layer extensionunnecessary in field situations (Montanaro et al., 2012) andreduces Eq. 3 to:

E ¼ gfruitwv VPD: (4)

4.4 Soil/Irrigation management and fruit mineralbalance

The leaves and fruits compete for xylem sap and the phloem-immobile nutrients therein. Hence, the absolute amount of Cacarried in the ascending sap and then distributed amongthese transpiring organs should ideally be as high as possibleto prevent limited Ca supply to any particular organ. This sec-tion discusses factors involved in the Ca-loading processesat the root–soil interface that may affect Ca delivery along thesoil–fruit pathway.

4.4.1 Soil and fertilization management

Roots absorb Ca2+ from the soil solution which is in equili-brium with the Ca bound to soil particles. This equilibrium isinfluenced by soil pH, cation exchange capacity and the rateof mineralization (McLaughlin and Wimmer, 1999). Increasingacidity promotes the release of structural Ca from soil par-ticles, for example, as soil pH drops below 5 substantialamounts of Ca oxalates readily dissolve (McLaughlin andWimmer, 1999). However, the effect of pH on Ca availability inthe soil solution is not linear; usually at soil pH < 4, Ca avail-ability for root uptake decreases because of the increased re-lease of Al, a strong competitor with Ca (McLaughlin andWimmer, 1999). In addition, at very low or high pH (i.e., < 3.0and > 9.0) Ca uptake may be completely blocked (Maas,1969). Considering that the chemical nature of nutrients sup-plied to the orchard may affect soil pH (Belton and Goh,1992, and references therein) it appears that an appropriatefertilization plan is required to avoid any negative impact onCa availability due to an unfavorable soil pH.

The mineral element balance in the soil is an additional possi-ble cause of Ca-uptake limitation because of the interactionsbetween nutrients. The antagonistic effect of high K on Ca up-take at the soil–root interface is a limiting factor for theamount of Ca loaded into the xylem at the root scale (Pathakand Kalra, 1971), with K fertilization inducing increased K tis-sue concentrations but depressing Ca concentrations (Fage-ria, 2001). For example, a reduction of 50% K supply induced

a higher Ca uptake in tomato fruit and lowered the incidenceof blossom end rot, increasing the marketable yield (Taylor etal., 2004). Therefore, it is advisable at least during the earlyfruit growth stage, when most of the fruit Ca is gained, that ex-cessive K supply should be avoided.

4.4.2 Root uptake

Calcium loading into the xylem occurs preferentially within theyoungest regions of the root axes where the suberized endo-dermal cells and Casparian strip have not yet differentiated orare temporarily disrupted by lateral root initiation (Harrison-Murray and Clarkson, 1973; Bangerth, 1979). This is be-cause the endodermal layer is a barrier to the apoplasmicpathway due to the hydrophobic chemistry of the Casparianband (White, 2001). Some evidence for symplastic movementof Ca is available for onion roots (Cholewa and Peterson,2004). It is likely that Ca enters the cytoplasm of the endoder-mal cells through Ca-permeable channels. Then it is activelytransported by specific antiporters at the stelar side, matchingthe need for low cytosolic Ca concentration (White, 2001).

In some kiwifruit-producing areas (e.g., Italy), conventional or-chard management includes frequent tillage to minimize com-petition for water between the crop and the spontaneousweeds (Testolin and Ferguson, 2009). This practice causes areduction in root density in the upper soil layer (Montanaro etal., 2007) where available Ca is higher (Jobbagy and Jack-son, 2001), hence, tillage may have a negative impact on Caabsorption. Calcium may also be accumulated at the rootapex in specialized cells that serve initially as a Ca sink andthen by remobilization as a Ca source, thereby accommodat-ing Ca demand from cell differentiation and root elongation(Storey et al., 2003). Therefore, we suggest avoidance of soildisturbance to maximize root Ca uptake particularly duringStage I of fruit growth when fruit Ca demand is high.

4.4.3 Irrigation

Calcium arrives at the root surface mainly through mass flow.The amount of nutrient supplied by mass flow is influenced bythe absorption of water by the plant and the ion concentrationof the soil solution (Kirkby, 1979). The most important processdriving mass flow is that of transpiration from the leaves,which establishes a water potential gradient downward to thesoil–root interface (Slatyer, 1960). Given the dependence ofCa uptake on water absorption (Kitano et al., 1999) and that astomatal limitation of transpiration occurs under reduced soilwater content (Miller et al., 1998), soil moisture should bemaintained at an optimal level, particularly during early fruitgrowth. Shading and reduced VPD should also be avoidedbecause they will cause reduced transpiration and Ca accu-mulation (Xiloyannis et al., 2003; Montanaro et al., 2009). Ithas been demonstrated that day-time irrigation decreased airtemperature and VPD of the maize canopy, whilst microcli-matic changes during night-time irrigation were minimal(Cavero et al., 2009). Hence, to promote day-time transpira-tion and Ca accumulation, we suggest irrigation at night whenthe VPD is already low. However, further research is neededto test this hypothesis in kiwifruit orchards.



Continuously high soil moisture (e.g., close to field capacity)may also be unfavorable for Ca nutrition. For example, over-irrigation will reduce the ion concentration in the soil solution,even though under these conditions more Ca is expected tobe available due to the increased bicarbonate content associ-ated with lower aeration (Wiersum, 1979). In conclusion, thereare a number of ways in which variations in soil water contentmay affect Ca supply. To avoid excessively low or high soilwater content we suggest that irrigation should be carefullymanaged according to the evaporative demand of the envi-ronment and the water-holding capacity of the soil volume ex-plored by the roots (Xiloyannis et al., 1993).

4.4.4 Fruit mineral balance

Levels of nutrients other than Ca or their ratios with Ca mayalso influence fruit quality traits (Marcelle, 1995). Potassiumhas several functions in berry growth including volume in-crease during cell-expansion (Mpelasoka et al., 2003);hence, high levels of K could uncouple fruit growth and Ca im-port causing dilution of fruit Ca (see Fig. 2). Moreover, K+

(and Mg2+) compete with Ca2+ for binding sites at the plasmamembrane, potentially negatively affecting membrane stabili-ty and increasing susceptibility to Ca deficiency disorders (DeFreitas and Mitcham, 2012, and references therein).

A high rate of nitrogen supply induces rapid growth and highvigor of shoots. This in turn increases leaf transpiration (dueto increased foliage surface area) resulting in more xylem Cadelivered to the leaf rather than to the fruit (Morandi et al.,2010). In vigorous avocado trees, Ca concentration in theflesh of mature fruit was 80% of that measured on non-vigo-rous trees (Witney et al., 1990). In apple trees higher annualnitrogen inputs (up to 150 kg ha–1) can increase fruit growthrate and final size, resulting in 30% lower fruit Ca concentra-tion when compared to unfertilized trees (Tahir et al., 2007).

In kiwifruit, high nitrogen supply has been associated with lowfruit-storage potential caused by more rapid fruit softeningduring storage. For example, Pacheco et al. (2008) reportthat an increased annual N supply from 30 to 90 kg ha–1 in-creased the mean N concentration of berries of kiwifruit from165 up to 190 mg per 100 g FW, which in turn induced ap-proximately 10% lower firmness. Similarly, in a 3-year experi-ment, high annual N supply levels (150–300 kg ha–1) resultedin leaf N concentration at harvest of 3% DM, while it was1.6% in unfertilized plots (Johnson et al., 1997). Leaf N con-centrations correlated negatively with fruit firmness. After 6months of storage, firmness values of fruit from unfertilizedplots were two-fold higher than those of fruits from the plotsreceiving high N supply (Johnson et al., 1997).

Low fruit Ca concentration is commonly cited as the maincause of higher incidence of several Ca-related disorders,and recently a role has even been proposed for localized (cel-lular level) Ca deficiencies (De Freitas et al., 2010). However,taking into account the direct and indirect effects of other nu-trients on Ca uptake and partitioning, information on nutrientconcentration ratios may also be used for better interpretationof fruit nutritional status. For that purpose, Table 1 provides arange of macronutrient concentrations and their ratios with Cain healthy fruits.

5 Internal factors

5.1 Fruiting shoot-type and leaf-to-fruit ratio

As observed for apple fruit, kiwifruit mineral concentrationvaries considerably according to fruit position within the cano-py and leaf-to-fruit ratios (Lang and Volz, 1998; Thorp et al.,2003). Usually, fruits grown near the trunk of kiwifruit vines(where leaf area density is highest) a higher leaf : fruit ratio


Table 1: Nutrient concentrations and nutrient ratios measured in healthy berries of kiwifruit at harvest.

Reference Clark andSmith, 1988

Benge et al.,2000

Smith et al.,1994

Montanaro etal., 2006

Buwalda andSmith, 1987

MEAN – SE

Nutrient concentration/ % DM

N 0.87 0.72 0.89 0.87 0.75 0.82 0.04

P 0.18 0.14 0.15 0.11 0.14 0.14 0.01

K 1.93 1.37 1.96 2.66 1.54 1.89 0.22

Ca 0.23 0.1 0.16 0.17 0.19 0.17 0.02

Mg 0.07 0.05 0.07 0.17 0.06 0.08 0.02

Ratios

N : Ca 3.78 7.20 5.56 5.12 3.95 5.12 0.62

P : Ca 0.78 1.40 0.94 0.65 0.74 0.90 0.13

K : Ca 8.39 13.70 12.25 15.65 8.11 11.62 1.48

Mg : Ca 0.30 0.50 0.44 1.00 0.32 0.51 0.13

(K + Mg) : Ca 8.70 14.20 12.69 16.65 8.42 12.13 1.59


positively influences fruit Ca accumulation (Thorp et al.,2003).

5.2 Fruit morphology and skin anatomy

The exocarp or skin of the fruit provides an important inter-face between the environment and the fruit itself, affordingprotection against pathogens and diseases, and moderatesevaporative water loss. As anticipated above, the diffusiveconductance of the fruit skin to water vapor is a major deter-minant of the transpiration rate, even though it operates inseries with the boundary layer conductance. Therefore, it ispredictable that any changes in the structure and function ofthe skin will affect fruit transpiration and import of phloem-im-mobile nutrients. The conductance of the kiwifruit berry skin istime-dependent and can be approximated as a simple expo-nential function of time from full bloom (Fig. 10, R2 = 0.87;Montanaro et al., 2012). Noticeably, conductance declinesrapidly during early fruit growth, and then remains relativelystable for the remainder of the season (Smith et al., 1995;Montanaro et al., 2006, 2012).

An earlier study of the skin of kiwifruit berry described the on-togeny and structure of covering trichomes (White, 1986).The Actinidia genus is characterized by simple (uniseriate)and complex (multiseriate) hairs, whose base protrudes fromthe fruit surface (Hallet and Sutherland, 2005). Early in fruitdevelopment the hairs are alive and probably increase the ef-fective fruit surface area and conductance to water vapor.However, by 50 DAFS the hairs are more suberized and theirviability has decreased by 90% (Xiloyannis et al., 2008), prob-ably contributing to the reduction in fruit surface conductanceand transpiration. By 6–8 weeks after fruit set—after the peri-od of fastest fruit expansion—the outer layers of the fruit forma periderm, with cell-wall suberization and cell collapse(Xiloyannis et al., 2001; Hallet and Sutherland, 2005; Celano

et al., 2009) further contributing to the decline in fruit surfaceconductance, transpiration and calcium accumulation (Figs.4, 5, and 10).

Fruit surface morphology may also be relevant for the efficacyof pre-harvest Ca applications. Foliar application of Ca is arecommended practice for fruit crops to reduce the incidenceof some Ca-related disorders even though they have erraticeffects on fruit Ca concentration and the incidence of disor-ders (Rosen et al., 2006; Yamane, 2014). After reviewing theevidence for deciduous fruit trees, Yamane (2014) invokedenvironmental conditions, particularly relative humidity andpre-existing within-canopy variability in fruit Ca content as thecauses of the variable response of fruit Ca concentration tofoliar Ca spray. However, the penetration of exogenous calci-um into fruit is also affected by the stage of fruit development.In three apple varieties, Schlegel and Schonherr (2002)found that the highest rates of penetration occurred duringthe early stages of fruit development (15–20 DAFS) whenclose to 100% of the applied CaCl2 penetrated after just 6 h.This percentage declined to 15% by 70 DAFS and 24 h wererequired for 20–40% penetration. In that experiment, the late-season decrease in the penetration rates was mainly associ-ated with the development of stomata into lenticels.

Accordingly, the penetration of Ca and its commonly usedtracer, strontium (Sr) (see Rosen et al., 2006) into the kiwifruitberry is affected by fruit age. After spray application of aque-ous solutions (0.16 M) of CaCl2 and SrCl2 to 35, 50, and150 d old Hayward kiwifruit, Cryo-SEM energy dispersiveX-ray microanalysis applied to frozen-hydrated samples ofthe outer layer of flesh revealed that no Ca or Sr penetratedthe fruit by 50 DAFS (Minnocci et al., 2007). This lack of pen-etration in kiwifruit compared to apple is possibly caused bythe lack of stomata on the kiwifruit skin (White, 1986) and theonset of the development of the suberized periderm aroundthis time.

5.3 Fruit hydraulic resistance

Variation in fruit xylem hydraulic resistance (the reciprocal ofhydraulic conductance) during fruit development was recentlyexamined in detail for kiwifruit (Mazzeo et al., 2013). Resist-ance declines quickly during early fruit growth, then increasesagain after » 60 DAFS (Fig. 11). Remarkably, late in the sea-son 90% of total hydraulic resistance was accounted for bythe receptacle zone. These ontogenetic changes mightcontribute to seasonal changes in xylem and mineral in-flowsinto the developing kiwifruit berry, including the reduced im-port of symplast-immobile ions such as Ca, and also to an in-creased import of symplastically transported species such assugar and potassium (Lang, 1983).

The reduction in fruit hydraulic resistance occurs in coordina-tion with the early stage of rapid increase in fruit volume(Stage I) when most of the fruit Ca is gained (Figs. 2 and 11)(Mazzeo et al., 2013). The rise in hydraulic resistance beginswith the second phase of fruit growth, long before fruit ripen-ing, confirming that the declining xylem inflows observed atthat time of the season (Morandi et al., 2010) are correlatedwith increasing hydraulic resistance. Reduced irradiance also


Cal

cula

ted

skin

con

duct

ance

G/ m

mol

cm

–2h–1

Ski

n co

nduc

tanc

e/ m

mol

cm

–2h–1

[Log

10]

Time / d AFS [Log10]

Figure 10: Skin conductance (G) to water vapor of berries of kiwifruitcalculated using the function G = E/DPw, where E is the fruit transpira-tion (mmol cm–2 h–1) and DPw (dimensionless) is the difference be-tween the water vapor (mol fraction) inside the fruit and that in thesurrounding atmosphere. In the inset: the fitted line is the estimatedconductance (G¢) versus time (t) in days after fruit set, using theequation G¢ = 13400 · t21.90; adjusted R2 = 0.87. Redrawn fromMontanaro et al. (2012).


causes an increase in berry xylem hydraulic resistance(Mazzeo et al., 2013), suggesting that the effect of reduced ir-radiance on mineral accumulation discussed above is causedby reductions in xylem inflows connected to changes in xylemdifferentiation and hydraulic resistance.

5.4 Transpiration-independent mechanisms

White and Broadley (2003) have stressed that a consistentrelationship between transpiration and Ca delivery to theshoot is usually only observed when the Ca concentration inthe xylem sap is high, anticipating that there is no simple pro-portional relationship between Ca delivery and transpiration.This is in accordance with several observations in tomato,bean and apple (Koontz and Foote, 1966; Bangerth, 1979;Banuelos et al., 1987; Pomper and Grusak, 1997), confirmingthat transpiration-Ca correlations are not always clear. Calci-um entering the apricot fruit did so by means of putative non-transpirational mechanisms including root pressure (Monta-naro et al., 2010), supporting the idea that transpiration is notthe only factor governing the movement of Ca. In that study itwas estimated that approximately 30% of the total Ca enter-ing the apricot fruit did so by means of putative non-transpira-tional mechanisms.

Partitioning of Ca amidst plant organs can also be attributedto a metabolic demand and the chemical aspects of the con-ductive tissues (e.g., sorption and desorption processes oc-curring at exchange sites along the walls of the xylem path-way; McLaughlin and Wimmer, 1999). Apart from the positiveeffect of auxin on induction and formation of vascular tissues(see for review: Ye, 2002), a mutual relationship between po-lar basipetal auxin transport and acropetal Ca transport hasbeen reported for tomato, apple and avocado (Stahly andBenson, 1970; Bangerth, 1976; Banuelos et al., 1987; Cut-ting and Bower, 1989). Involvement of seeds in the mechan-ism seems to be plausible. Using parthenocarpic apple fruit,Bangerth (1976) concluded that endogenous auxins, possiblysynthesized in the seeds, play a significant role for Ca nutri-

tion of fruits. For kiwifruit, such information is not available,however, a correlation (R2 = 0.92) between auxin and Ca con-centrations has been reported; even though, any possiblecausal mechanism remains to be elucidated (Sorce et al.,2011).

Results from supplementary pollination experiments supportthe concept of a mutual relationship between auxin and Catransport. That is, poor pollination reduces seed number andCa concentration on a whole-tree basis in Braeburn applefruit (Brookfield et al., 1996; Volz et al., 1996). In kiwifruit, highseed number, fruit size and dry matter content are achievedby ensuring high levels of pollination. Howpage et al. (2001)showed that the mean seed numbers (in comparable fruit sizeclasses) from higher weight groupings (i.e., 70–89, 90–109,and 110 g per fruit) in bee-supplemented vines was signifi-cantly higher than that in non-bee pollination treatment.Therefore, it is plausible that ensuring good pollination (e.g.,by bee or artificial pollen application) would be beneficial forseed number and in turn Ca accumulation.

6 Conclusions

This review highlights that 80% of the total Ca content of thekiwifruit berry are gained within the early weeks after fruit-set,suggesting that failure of good fruit Ca nutrition at this timemay easily lead to poor fruit Ca at harvest. Therefore, to en-hance Ca accumulation by fruit during the early fruit growthstage, we recommend a series of practical steps:

– Do ensure good pollination to promote high seed numbersper fruit.

– Limit nitrogen fertilization to prevent excess vegetativegrowth that competes with the fruit for water and Ca and re-duces irradiance within the canopy.

– Do not apply excessive K because of its antagonistic effecton Ca uptake by the roots.

– Summer prune to (1) avoid development of highly vigorousshoots and (2) promote irradiance within the canopy and inturn higher fruit xylem conductance.

– Do not till the soil so that roots remain functional in theupper Ca rich soil layer.

– If Ca supplements are to be applied, do so before 50 DAFSbefore their penetration rate declines as a result of the suberi-zation the fruit periderm.

– Manage irrigation to prevent under- or over-irrigation andimpairment of root Ca uptake; introduce night-time irrigationto avoid reduced within canopy day-time VPD and fruit tran-spiration throughout early fruit development.

Acknowledgment

The study was financially supported by the Italian Ministry ofUniversity and Scientific Research Special grant PRIN2009,and by the Project PSR Basilicata 2007–2013, Misura 124,OTIROL.


Tota

l fru

it hy

drau

lic re

sist

ance

x 1

0–3

/ MPa

s g

–1

Figure 11: Seasonal changes in total hydraulic resistance measuredusing the flowmeter method on A. deliciosa cv. ‘Hayward’ kiwifruit.Values are the means – SE of 12 fruits. Redrawn from Mazzeo et al.(2013).


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