Activities of Enzymes Directly Related With Sucrose and Citric Acid

8/10/2019 Activities of Enzymes Directly Related With Sucrose and Citric Acid

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Scientia Horticulturae 168 (2014)7380

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Scientia Horticulturae

journal homepage: www.elsevier .com/ locate /scihor t i

Activities ofenzymes directly related with sucrose and citric acidmetabolism in citrus fruit in response to soil plastic film mulch

NiJianga, Long-FeiJin a,Jaime A. Teixeira da Silvab, MD Zahidul Islam a, Hai-Wen Gaoa,Yong-Zhong Liua,, Shu-Ang Penga

a Key Laboratory of Horticultural Plant Biology (HuazhongAgriculturalUniversity),Ministry of Education, Wuhan 430070, Peoples Republic of Chinab P.O. Box7,Miki-cho Post Office, Ikenobe 3011-2, Kagawa-ken 761-0799,Japan

a r t i c l e i n f o

Article history:

Received 28October 2013

Received in revised form 7 January 2014

Accepted 16 January 2014

Keywords:

Citric acid-metabolizingenzymes

Fruitquality

Mulch cultivation

Sucrose-metabolizingenzymes

a b s t r a c t

Soil plastic film mulch is commonly employed in citrus production regions ofEast Asia to improve fruit

quality. In the present study, Ponkan tangerine (Citrus reticulata Blanco) was mulched under the tree

canopy with silver-black reflective film during fruit development. At about 12 days after mulching, total

soluble sugar and citric acid contents in the segment membrane and/orjuice sacs offruit frommulched

trees increased significantly relative to the control. Inthe segmentmembrane, the activities ofacid inver-

tase (AI) and sucrose synthase (SS; cleavage direction) increased significantly followingmulch treatment.

However, the activities ofother enzymes, includingneutral invertase, SS (synthetic direction) andsucrose

phosphate synthase did not respond significantly under mulch treatment. In the juice sacs, SS activity

(cleavage direction) frommulched treatments was significantly lower than that from control trees while

SS activity (synthetic direction) frommulched treeswassignificantly higher than that from control trees.

Moreover, the activities ofcytoplasm aconitase (cyt-Aco) and isocitrate dehydrogenase (cyt-IDH) were

significantly lower thanthose in the control fruits after 36 days ofmulching. In conclusion, the activities

ofSS (synthetic direction) and AI were significantly enhanced while those ofcyt-Aco and cyt-IDH were

significantly reduced by soil plastic film mulch. A schematic model is present indicating the possible

important roles that these key enzymes play in sugar and acid accumulation in citrus fruits under soil

plastic film mulch. 2014 Elsevier B.V. All rights reserved.

1. Introduction

Citrus is one of themost important fruit crops in theworld with

an annual production exceeding 122.5 million tons in 2010 (FAO-

STAT2012). The periodof fruit ripening is often in the rainy season

inEast Asiancitrus production regions. Thus, soil plastic filmmulch

(SPFM) is commonlyemployedtocontrolsoilhumidityby prevent-

ing rainwater from entering into the soil, and is a proven effective

soil management practice for theimprovement of fruit quality (Shi

et al., 2011; Yakushiji et al., 1996).SPFM is a soilmanagement practicewidely used in the produc-

tion of vegetable and field crops (Kasirajan and Ngouajio, 2012;

Abbreviations: Aco, aconitase; AI, acid invertase; CS, citrate synthase; cyt-Aco,

cytoplasm aconitase; cyt-IDH, cytoplasm isocitrate dehydrogenase; IDH, isocitrate

dehydrogenase; mit-Aco, mitochondrial aconitase; NI, neutral invertase; PEPC,

phosphoenolpyruvate carboxylase; SPS, sucrose phosphate synthase; SPFM, soil

plastic filmmulch; SS, sucrose synthase; SS-CD, sucrose synthase-cleavage direc-

tion; SS-SD, sucrose synthase-synthetic direction;TSS, total soluble sugar. Corresponding author. Tel.: +8627 87281897; fax: +8627 87282010.

E-mailaddresses: [email protected], [email protected](Y.-Z. Liu).

Lament, 1993), as well as fruit crops (Dusek et al., 2010; Glenn

and Puterka, 2007; Layne et al., 2001; Yakushiji et al., 1996). The

widespreadapplicationand importanceoffilmmulchin agriculture

is because it canimprove themicroclimatearounda plant by regu-

latingmoisture, temperature, light and energy exchange (Heiner

et al., 2005;Tarara, 2000). The use offilmmulch has beenshown to

increase fruit soluble solids, total phenolics, flavanols, and antho-

cyanins in many fruit crops, including grape (Vitis vinifera L.) (Liu

et al., 2008), strawberry (FragariaaranassaDuch.) (Loughrin and

Kasperbauer, 2002; Wang and Millner, 2009), peach [Prunus per-

sica (L.) Batsch] (Layne et al., 2001), apple (MalusdomesticaBorkh.)

(Glenn and Puterka, 2007; Iglesias and Alegre, 2009) and pineap-

ple (Ananas comosus L.) (Dusek et al., 2010). Fruit aroma was also

increasedby filmmulch in strawberry (LoughrinandKasperbauer,

2002) and pineapple (Liu et al., 2011). Citric acid content can also

be increased in strawberry by filmmulchwith black plastic mulch

(WangandMillner, 2009) butwhensilver-blackreflectingfilmwas

used, the titratable acid content decreased in loquat [Eriobotrya

japonica (Thunb.) Lindl.] (Chen et al., 2010). In a citrus, Satsuma

mandarin (Citrus unshiu Marc.), Yakushiji et al. (1996) found that

mulch with micro-perforated vinyl sheets decreased soil water

0304-4238/$ seefrontmatter 2014 Elsevier B.V. All rightsreserved.

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74 N. Jiang et al./ Scientia Horticulturae 168 (2014) 7380

potential, but increased sugar content and fruit acidity. Shi et al.

(2011) also found that vapor-permeable reflective filmmulch and

silver-black reflecting film mulch increased soluble solids signif-

icantly, but had no significant effect on fruit acidity of Ponkan

tangerine (Citrus reticulata Blanco).

Although film mulch has a positive effect on fruit quality, only

few studies have investigated the possible reason for this impact.

For example, Liu et al. (2008) suggested that an increase in acid

invertase (AI; EC 3.2.1.26) activity plays an important role in the

increasein sugar accumulationin grape fruitunderblueplasticfilm

mulch. Improvement of the microclimate, including an increase in

light intensity and canopy air temperature as well as a reduction

in canopy relative humiditywas attributed to the improvement of

apple (Layneet al., 2001) and peach (Glenn andPuterka, 2007) skin

coloration. The contents of soluble sugar, titratable acid and their

ratio are important for citrus fruit flavor quality (Zhouet al., 1985).

Eventhoughcitrusfruitsugar and acidcontentscanalsobe affected

by filmmulch (Shi et al., 2011; Yakushiji et al., 1996), knowledge

of the underlying mechanism(s) remains scant.

It is well known that citrus fruit sugar is transported in the

form of sucrose from source leaves and that pulp acidity is syn-

thesized in fruit cell mitochondria through the incorporation of

acetyl-CoA with oxaloacetate, a reaction catalyzed by citrate syn-

thase (CS; EC 2.3.3.1), and then translocated to and stored in thevacuole(Sinclair,1984). Sucrose partitioninto fruitis mainlydeter-

minedbysink strength,which is thecompetitive ability ofanorgan

to attract assimilates (Marcelis, 1996) and is mainly related to the

ability of sucrose-metabolizing enzymes, suchas sucrose synthase

(SS; EC 2.4.1.13) and invertase (EC 3.2.1.26), to hydrolyze sucrose

(Koch, 2004).Ontheotherhand, fruitpulp acidity isdirectly related

withcitricacidcontent (Sinclair,1984),whichis determined by the

balance in activity of phosphoenolpyruvate carboxylase (PEPC; EC

4.1.1.31), CS, aconitase (Aco; EC 4.2.1.3) and isocitrate dehydro-

genase (IDH; EC 1.1.1.41). Aco activity plays an important role in

determining the accumulation of citric acid in the vacuole (Cercs

et al., 2006; Sadka et al., 2000).

In this paper, we investigated the activities of all the enzymes

directly related with sucrose and citric acid metabolism in cit-rus fruit juice sacs and/or segment membrane under SPFM. These

enzymes aresucrose phosphatesynthase (SPS; EC2.4. 1.14), SS, AI,

neutral invertase(NI), PEPC, CS,mitochondrialAco (mit-Aco), cyto-

plasmicAco(cyt-Aco) andcytoplasmicIDH (cyt-IDH).Theobjective

of this studywas to identify enzymatic factors involved in increas-

ing soluble carbohydrate and acid accumulation in citrus fruit in

response to SPFM during fruit development and ripening.

2. Materials and methods

2.1. Plant materials and treatment

Experiments were performed on 6-year-old Ponkan (C. reticu-

lata cv. Egan 1

) trees grafted on Poncirus trifoliata at the citrusorchard of Huazhong Agricultural University in 2011. Citrus fruit

development was divided into three stages: cell division, rapid

growth period and maturation (Bain, 1958). The beginning of the

rapidgrowth periodof Ponkanis aboutearlyAugustin theresearch

area. During the rapid fruit growth period (August 18, 2011), six

healthy, approximately uniform and fruitful trees were selected

and irrigated well with about 50L of water per tree. Then, a plot

containingthreetrees(i.e., three replicates)wasfullyoverlaidwith

silver-black reflective film (Qingdao Aolong plastic products Co.,

Ltd. China)whileanotherplot, also containingthreeother treesnot

covered with film, served as the control. Two guard rows of citrus

trees separated the two plots. The silver-black reflective film cov-

ered the soil under the tree crown tightly to protect rainfall from

permeating into the mulched soil. After film mulching, irrigation

was paused for mulched trees while control trees were irrigated

normally, i.e., once (about 50L of water per tree) a week if no rain

fell. A total of 2530 mature leaves per tree were collected ran-

domly from spring shoots every 24 days while 610 fruits were

randomly collected from the outer crown of each tree every 12

days. Thesegmentmembrane andjuice sacs of fruitsfromeach tree

were separated and the same tissue was then pooled. Some juice

sacs were used fresh to determine total soluble solid content. The

remainingsampleswerefrozen in liquidnitrogen, thengroundinto

granules andstored at80 C to determine sugar and acid content

and to analyze related enzymeactivity.

2.2. Measurement of water status

Soil waterpotentialwasmeasuredbya soil tensionmeter (TEN-

30, Zhejiang Top Instrument Co., Ltd., Hangzhou, China). The soil

tensionmeter,onepertree,wasburied30 cmunderthesoil surface

10cm from the tree canopy drip line. Data was collected between

9:00 and 10:00a.m. Leaf water potential was measured by a plant

pressure chamber (ARIMAD-3000, Israel) according to the man-

ufacturers instruction manual. Six mature leaves were randomly

collected from the spring shoots of the outer canopy of each tree.

Leaves sampled fromthe six trees were located at almost the same

height and orientation. They were collected at predawn (about6:00a.m.) tominimize theeffect of transpiration on thewater sta-

tus of plants.

2.3. Measurement of net photosynthetic rate

The net photosynthetic rate of leaves was measured with a

portable photometer (Li-6400, USA). Measurementsweremadeon

healthy mature leaves from the middle of spring shoots of each

plant (10 random leaves per tree) 48 days after mulch treatment.

Allmeasurements were carried out between 09:00 and 11:00a.m.

under an air CO2 concentration of 38510molmol1.

2.4. Determination of leaf proline

Proline was determined every 24 days according to a spec-

trophotometric method (Li, 2000). Approximately, 0.5g of leaf

granules was homogenized in 10mLof 3% aqueous sulfosalicylic

acid. The homogenate was filtered through Whatman #2 filter

paper into a clean 15-mL centrifuge tube. 2mL of filtrate was

reacted with 2mLof glacial acetic acid and 2mL of acid ninhydrin

in a 15-mL centrifuge tube for 30min at 100 C. After the reaction

was terminated in an ice bath, the filtrate was extractedwith 4mL

of toluene and mixed vigorously for about 30s and centrifuged at

3000gfor 5min. The supernatant was used to detect proline at

520nmwith a UV-1600 Shimadzu spectrophotometer (Japan).

2.5. Determination of total soluble solids, starch, soluble sugar,

citric acid and malic acid contents

Fruittotalsolublesolidscontent(expressedasapercentage)was

determined using a common laboratory refractometer (Chengdu

Tech. Co., Ltd., China). Leaf total soluble sugar (TSS) and starch

were determined using thephenol-sulfuric acid methodandacid-

hydrolyticmethod (Li,2000), respectively. Soluble sugars (glucose,

fructoseandsucrose) andcitric acidweredetermined bygas-liquid

chromatography (Bartolozzi et al., 1997).

2.6. Enzyme activity assay

All procedures related to enzyme extraction were carried out

at 4 C or lower. The extraction of sucrose-metabolizing enzymes

and activity assays were determined by the method of Lowell


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N. Jiang et al. / Scientia Horticulturae 168 (2014) 7380 75

Fig.1. Changes ofwaterpotential(kPa)in thesoils ofSPFM(soil plastic filmmulch)-

treated andCK (control) trees. Asterisk (*) between or on bars indicates significant

differences between fruits of SPFM and CK at the same sampling point at P


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which it enters the juice sacs (Lowell et al., 1989). SPFM did not

change the trend (i.e., accumulation of TSS) in the segment mem-

brane, which increased as fruit developed, reached a maximum at

earlymaturation (48days after SPFM) and then decreased towards

the end of the experimental period. However, TSS concentration

in the segment membrane from mulched trees was significantly

higher after 38 days after SPFM than the level observed in con-

trol trees (Fig. 2A). In the juice sacs, SPFM obviously increased

the total soluble solids and TSS (sucrose, glucose and fructose)

contents at about 14 days after SPFM compared to the control

(Fig. 2BE).

Sucrose-metabolizing enzymes in boththe segmentmembrane

and juicesacswere analyzedduring themulchingperiod (Fig.3). In

the segment membrane, the activities of AI (Fig. 3A) and SS (cleav-

age direction) (Fig. 3C) increased significantly in response to SPFM

whereas the activities of other enzymes, including NI (Fig. 3B), SS

(synthetic direction) (Fig. 3D) and SPS (Fig. 3E) changed little after

mulching compared to the control. In the juice sacs, except for SS

activity, the activities of AI (Fig. 3F), NI (Fig. 3G) and SPS (Fig. 3J)

were only slightly affected by SPFM. SS activity of the cleavage

direction from mulched trees was significantly lower than that

of control trees (Fig. 3H), while the SS activity of the synthetic

direction frommulched trees was significantly higher than that of

control trees (Fig. 3I).

3.3. Changes in acid accumulation and activities of citric acid

metabolizing enzymes in fruit juice sacs

Since citric acid accounts for most of the acidity in citrus juice,

the concentration of citric acid was determined throughout the

mulching period (Fig. 4A). Citric acid accumulated during the

second stage of fruit development, peaked at about 12 days after

SPFM, and then declined gradually as the fruit matured. However,

after about 24 days of mulching, the concentration of citric acid

from fruits of mulched trees was significantly higher than that of

control trees.

The activities of enzymes directly related with citric acid syn-

thesis (PEPC and CS) and degradation (Aco and IDH) were also

investigated. Under normal conditions, PEPC activity decreased

continuously as fruit developed and matured (Fig. 4B) while CS

activity increased during the second phase of fruit development,

peaked in the middle of September and then declined as fruit

matured (Fig. 4C). Moreover, the activities of the two enzymes

(Fig. 4B and C) did not change much after SPFM compared to the

control. The activities of Aco and IDH increased as fruit developed

and matured (Fig. 4DF). SPFM did not change mit-Aco activity

appreciably (Fig. 4D) but decreased the activities of cyt-Aco and

cyt-IDHwhich were significantly lower than levels in control fruits

after about 40 days after SPFM (Fig. 4E and F).

Fig. 2. Sugar content in fruits in soil plastic filmmulch (SPFM) and control (CK) treatments. (A) Total soluble sugars in segment membrane. (B) Total soluble solids in juice

sacs. (C) Sucrose in juice sacs. (D)Glucose in juice sacs. (E)Fructosein juice sacs. Asterisk (*) between or on bars indicatessignificant differences between fruitsof SPFM and

CK at the same sampling point at P


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Fig.3. Activitiesof acidinvertase (AI),netural invertase(NI),sucrosesynthase-cleavagedirection(SS-CD),sucrose synthase-syntheticdirection(SS-SD)andsucrosephosphate

synthase (SPS) in fruit segmentmembrane and juice sacs in soil plastic filmmulch (SPFM) andcontrol (CK) treatments. Asterisk (*) between or on bars indicates significant

differences between fruits of SPFM andCK at thesame sampling point at P


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Fig. 4. Content of citric acid and activities of phosphoenolpyruvate carboxylase (PEPC), citrate synthase (CS),mitochondrial aconitase (mit-Aco), cytoplasmaconitase (cyt-

Aco) andcytoplasm isocitrate dehydrogenase (cyt-IDH)in fruit juice sacs between soil plastic filmmulch(SPFM) andcontrol (CK) treatments. Asterisk (*)betweenor onbars

indicatessignificant difference between fruits of SPFM andCK at thesame sampling point at P


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Fig. 5. A schematic model showing the response of key enzyme activities involved in sucrose and citric acid metabolism in response to soil plastic filmmulch. Grey wide

upright anddownright arrows show thepositive andnegative impact bymulch treatment, respectively.

confirmed that increased SS activity of the sink organ can increase

photoassimilate partition.

SPFM during citrus fruit development or maturation produced

mild drought stress in plants (Yakushiji et al., 1996), implying

that it might increase sugar accumulation in fruit juice sacs by

a mechanism similar to mild drought stress. The citrus fruit seg-

ment membrane is the site for photoassimilate downloading from

the phloemwhich then enters into juice sacs (Lowell et al., 1989).

In the present study, the TSS content and activities of sucrose

metabolizing enzymes in the segment membrane and juice sacswere analyzed separately. We found that TSS was significantly

enhancedbymulch treatmentunder drought stress (Figs. 1 and 2),

implying that photoassimilate partition into fruit juice sacs actu-

ally increased, similar to theresponseof drought-stressedSatsuma

mandarin (Yakushiji et al., 1998). Moreover, it was interesting to

note that theSS activity of cleavage directionandAI increased sig-

nificantly in the segment membrane while, in the juice sacs, the

SS activity of cleavage direction decreased significantly and that

of synthetic direction increased significantly when drought stress

occurred under mulch treatment (Figs. 1 and 3). In general, most

sucrose downloaded from the phloemwill be cleaved into glucose

and fructosebySS andcellwall invertase(a sub-setofAI) invascular

bundles of segment epidermisand then translocatedto cytoplasm,

mainly through sugar transporters (Liu, 2012). In the cytoplasm,some glucose andfructosewill form sucrose again, catalyzed by SS

(synthetic direction) andSPS, and then translocate to and be stored

in the vacuole (Koch and Avigne, 1990). Hence, we hypothesize

that theenhancement of SS (cleavagedirection) and AI activities is

the main reason for the increase of TSS in the fruit segment since

they increase the sink strength for sucrose partition into fruit. In

contrast, the increase in SS activity of synthetic direction and the

decrease in SS activity of cleavage direction lower hexose concen-

tration in the cytoplasm since SS (both directions) is conducive to

the transport of glucose and fructose from the segment epider-

mis into the cytoplasm, after which more sucrose is synthesized

by the increase of SS-SD activity in the cytoplasm and then may

be transported to and stored in the vacuole (Fig. 5). Based on the

present data, we conclude that the increase in sugar accumulation

inthe juicesacsundermulch treatmentcanalsobe attributed tothe

increase in sink strength through increased SS activity of cleavage

direction and AI activity in the segment membrane andSS activity

of synthetic direction in the juice sacs, anddecreased SS activity of

cleavage direction in the juice sacs.

Apart from sugar accumulation, citrus fruit acidity was also

affected bymulch treatment. In citrus fruit, the pathway ormech-

anism of citric acid accumulation and utilization in citrus fruit is

relatively clear (Cercs et al., 2006; Katz et al., 2007; Sadka et al.,

2000). However, even though some researchers found that fruitacidity was obviously increased by mulch treatment (Yakushiji

et al., 1996), deficit irrigation(Garca-Tejeroet al.,2010) ordrought

stress (Hockema and Etxeberria, 2001; Yakushiji et al., 1998), lit-

tle knowledge is available about how citrus fruit acidity can be

influenced throughmulch cultivation, deficit irrigationor drought

stress.In loquat, underSPFM,Chenetal.(2010) found that the total

organic acid concentration in fruit pulp was significantly higher

than that incontrol fruitpulp less than45daysafterSPFM,and then

theacidconcentrationdecreasedand becameobviouslylower than

the acid level in the control towards the end of mulch treatment.

By investigating changes in the activities of malic acid-related

enzymes, they concluded that the change in fruit pulp acidity

resulted primarily from the fluctuation inmalatecontent,with the

highercontentof organic acid during early stagesof mulchapplica-tion being attributed to an increase in both PEPC and NAD-malate

dehydrogenase activities and a decrease in NADP-malic enzyme

activity whereas the lower content of organic acid during the late

stage of mulch application was attributed to a decrease in both

PEPC andNAD-malate dehydrogenase activities andan increase in

NADP-malic enzymeactivity. In the present study,we also investi-

gated the probable enzymaticmechanism controlling fruit acidity

under SPFM. SPFM significantly decreased the activities of cyt-

Acoandcyt-IDH when drought stress occurredwhile interestingly

the activities of other enzymes, including PEPC, CS and mit-Aco,

showed no differences (Fig. 4). It is well known that cyt-Aco and

cyt-IDH are the key enzymes for citric acid utilization during fruit

ripening(Cercset al., 2006;Sadkaet al., 2000).Althoughthe signif-

icant reduction occurred about ten days later than the significant


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