This article was downloaded by: [East Carolina University] On: 24 September 2013, At: 00:03 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Plant Nutrition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/lpla20 Influence of rootstock on nutrient acquisition by pistachio P. H. Brown a , Qinglong Zhang a & Louise Ferguson a a Department of Pomology, University of California, Davis, CA, 95616–8683 Published online: 21 Nov 2008. To cite this article: P. H. Brown , Qinglong Zhang & Louise Ferguson (1994) Influence of rootstock on nutrient acquisition by pistachio, Journal of Plant Nutrition, 17:7, 1137-1148, DOI: 10.1080/01904169409364794 To link to this article: http://dx.doi.org/10.1080/01904169409364794 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article was downloaded by: [East Carolina University]On: 24 September 2013, At: 00:03Publisher: Taylor & FrancisInforma Ltd Registered in England and Wales Registered Number:1072954 Registered office: Mortimer House, 37-41 Mortimer Street,London W1T 3JH, UK
Journal of Plant NutritionPublication details, including instructions forauthors and subscription information:http://www.tandfonline.com/loi/lpla20
Influence of rootstock onnutrient acquisition bypistachioP. H. Brown a , Qinglong Zhang a & LouiseFerguson aa Department of Pomology, University ofCalifornia, Davis, CA, 95616–8683Published online: 21 Nov 2008.
To cite this article: P. H. Brown , Qinglong Zhang & Louise Ferguson (1994)Influence of rootstock on nutrient acquisition by pistachio, Journal of PlantNutrition, 17:7, 1137-1148, DOI: 10.1080/01904169409364794
To link to this article: http://dx.doi.org/10.1080/01904169409364794
PLEASE SCROLL DOWN FOR ARTICLE
Taylor & Francis makes every effort to ensure the accuracy of allthe information (the “Content”) contained in the publications on ourplatform. However, Taylor & Francis, our agents, and our licensorsmake no representations or warranties whatsoever as to the accuracy,completeness, or suitability for any purpose of the Content. Anyopinions and views expressed in this publication are the opinions andviews of the authors, and are not the views of or endorsed by Taylor& Francis. The accuracy of the Content should not be relied upon andshould be independently verified with primary sources of information.Taylor and Francis shall not be liable for any losses, actions, claims,proceedings, demands, costs, expenses, damages, and other liabilitieswhatsoever or howsoever caused arising directly or indirectly inconnection with, in relation to or arising out of the use of the Content.
This article may be used for research, teaching, and private studypurposes. Any substantial or systematic reproduction, redistribution,reselling, loan, sub-licensing, systematic supply, or distribution in anyform to anyone is expressly forbidden. Terms & Conditions of accessand use can be found at http://www.tandfonline.com/page/terms-and-conditions
In California, the pistachio industry uses three major rootstocks selected for
their vigor and/or resistance to disease (Verticillium wilt and root knot nematode).
These rootstocks are Pistacia atlantica (P. atlantica), Pistacia integerrima (P.
integerrima), and Pistacia integerrima x atlantica (PGII). Several other rootstocks
are also used, including Pistacia terebinthus (P. terebinthus), and Pistacia atlantica
x integerrima (UCBI). All pistachio rootstocks are produced from seed, generally
from a small number of parent trees.
Evidence that choice of rootstock can influence pistachio productivity has been
reported in both scientific and industry publications. Rootstock choice has been
shown to influence salt tolerance (Walker et al., 1987; Behoudian et al., 1986;
Picchioni et al., 1990), disease resistance (Ashworth, 1985), and vigor and
bearing habit (Crane and Iwakiri, 1987). We are not aware of any reference to the
nutrient efficiencies of the various pistachio rootstocks.
The role of rootstock selections in nutrient uptake by commercial species has
been reviewed by many authors (Embleton et al., 1973; Wutscher, 1973, 1989).
Use of a given rootstock based solely on nutritional characteristics, however, is
rare and has been limited to selection of iron (Fe)-chlorosis resistant and salt
[sodium (Na), chloride (Cl), or B] resistant citrus and peach rootstocks
(Wutscher, 1973). Rootstock characteristics such as disease and frost resistance,
precocity and size control are the key determinants of rootstock choice. The low
cost of inorganic fertilizers has meant that choice of rootstocks based solely on
nutritional characteristics can only be justified for the most intractable nutritional
problems. Several such intractable problems exist in commercial pistachio
production.
Within the extensive pistachio growing regions of California, deficiencies of
nitrogen (N), Cu, B, and Zn are the most common. Whereas N deficiencies can be
adequately corrected with the addition of fertilizer N, deficiencies of Cu, Zn, and
B are less amenable to such solutions. Many soils on which pistachio is grown are
characterized by high pH and carbonate content, low organic matter, and high clay
content. In these soils, deficiencies of Zn and Cu can become severe, resulting in
the development of characteristic symptoms of delayed bud break, impaired
growth of meristematic regions and significant yield loss. Frequently where
deficiencies are observed, soil applications of Zn or Cu either as inorganic salts or
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NUTRIENT ACQUISITION BY PISTACHIO 1139
chelated compounds is ineffective (Brown et al., 1991). Pistachio is notoriously
inefficient at the absorption of foliar applied Zn and Cu, a problem thought to be
associated with the low penetration and high complexing capacity of the leaf
waxes (Brown et al., 1991). Boron can be supplied as either a soil amendment or
foliar spray to pistachio. Timing of B foliar sprays is critical and there is a danger
of B toxicity from excessive sprays (Brown et al., 1992). As a result of these
physico-chemical and practical problems, deficiencies of Zn, Cu, and B are not
reliably corrected by soil or foliar application of fertilizers. The use and further
selection of rootstocks better able to supply these nutrients to pistachio under a
range of soil conditions would be of great practical and economic significance.
MATERIALS AND METHODS
Six commercial pistachio orchards were identified in 1990. At four of these
sites, the commercial cultivar 'Kerman' was grafted on a variety of the major
pistachio rootstock cultivars. At two additional sites, nutrient element concen-
trations in leaves of two-year-old seedling rootstock trees (non-grafted) were
determined. The sites used in these experiments represent a range of climatic and
soil conditions within California and ranged in soil texture from fine sandy loam to
heavy clay loam, soil pH varied from 5.5 to 8.0, and tree age varied from two
years old (for seedling rootstocks) to thirty years. All trees were irrigated with
microsprinklers and fertilization was uniform at all sites. One hundred and fifty
kilograms of nitrogen (N), 100 kg potassium (K), and 50 kg phosphorus (P) were
applied to each hectare as liquid fertilizer in two applications, 60% in late fall, 40%
in spring through the irrigation system. In addition, foliar Zn (3.5 kg Zn/ha) was
applied to site three in spring. Sites differed significantly in soil type, irrigation
supply, crop management, and climatic conditions.
At each of these sites, plantings of 'Kerman' scions on a variety of rootstocks
were available. The rootstocks investigated here include: P. atlantica, P.
terebinthus, P. integerrima, and Pistacia integerrima x atlantica (PGII), and
Pistacia atlantica x integerrima (UCBI). Though the exact experimental design
differed between sites, each site did contain at least four of the rootstock species.
Each site contained at least 20 replicate trees per rootstock. At each site, twenty
trees of each rootstock were chosen at random from within the larger rootstock
trial. Thirty non-terminal leaflets were collected from the youngest fully expanded,
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1140 BROWN, ZHANG, AND FERGUSON
non fruiting spurs around the periphery (2.0 m height). Leaves were washed with
mild detergent and then rinsed with de-ionized water before drying for 48 hrs a
70°C. Leaf tissue was then ground to pass a 40-mesh screen, dry ashed (550°C),
resuspended in 0.1N HNO3, and analyzed for Cu, B, Zn, Mn, Fe, Mg, P, and Ca
by ICP (ARL 3500, Sunland, CA). Trees were selected for uniformity of size and
crop yield.
All data were evaluated statistically by analysis of variance techniques. Means
separations were performed by Fishers protected LSD (Statview and SuperAnova
Statistical Programs, Abacus Concepts, Berkeley CA). Correlation analysis was
then performed to determine if efficiency in uptake of one element was signi-
ficantly correlated with efficiency in uptake of a second element that may suggest a
common mechanism for acquisition of both elements.
RESULTS
The use of several different locations in this experiment allows us to make
conclusions on the overall nutrient efficiency of the various rootstocks. Leaf
elemental concentrations differed significantly between sites and resulted in
variations in the degree to which rootstock choice affected plant response (Tables
la and lb). To illustrate this point and provide an overall comparison of
rootstocks, data for all sites is presented. Rootstocks were ranked at each site for
nutrient concentration, and statistical differences determined (Tables la and lb).
All comparisons of rootstock effects reported here were made on leaf samples
collected in July which is the normal leaf sampling date. Analysis of other
sampling dates reveals that differences in rootstock nutrient efficiency was evident
at all sampling dates (not shown), however, since the available critical values for
each nutrient have been established for July samplings, we will restrict our
discussion to this period. In the following, rootstock responses are discussed in
relation to each of the nutrient elements measured.
Magnesium: Significant differences in Mg content of scion leaves was
observed (Table la). Pistachio growing on 'Terebinthus', 'UCBI1, 'BGII', or
'Integerrima' had higher Mg contents than those growing on 'Atlantica1. Leaf Mg
concentrations of less than 0.5% are considered deficient (Beutel et al., 1972). At
leaf Mg concentrations below 0.5%, rootstock has a significant effect on leaf Mg
concentrations, while above 0.5% leaf Mg, the differences are not significant.
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NUTRIENT ACQUISITION BY PISTACHIO 1141
TABLE 1a: Macro-Nutrient Concentrations in Leaves of Grafted 'Kerman' and Non-Grafted Pistachio.
ElementPhosphorus
(%)
Calcium(%)
Magnesium(%)
RootstockAtlanticaIntegerrimaPGIIUCBITerebinthus
AtlanticaIntegerrimaPGIIUCBITerebinthus
AtlanticaIntegerrimaPGIIUCBITerebinthus
Site1
0.16a0.12b0.13b0.16a
1.3a2.2b
2.02b1.46a
0.38b0.49a0.49a0.42a
GraftedSite
20.160.140.150.14
1.25a1.7b
1.32a1.74b
0.38b0.42a0.4a
0.53a
TreesSite
30.14a0.12b
0.13a0.12b
33.5
2.63.1
0.560.51
0.460.49
Site4
0.130.13
0.120.12
1.7a1.9a
1.1b1.5b
0.670.73
0.820.65
Non-GraftedSite
50.16a0.11b0.13b0.15a
1.4a2b
1.6a1.6a
0.38b0.49a0.49a0.42a
TreesSite
60.130.140.130.12
1.21.41.61.4
0.32b0.40a0.41a0.42a
All values are the means of 20 trees sampled in JulyNumbers with different letters differ significantly (P<0.05)* = probable contamination
Phosphorus: Differences in P concentration were most marked at higher Pvalues (Table 2). P. atlantica was the most effective rootstock followed by'UCBI', with 'PGII' and 'Integerrima' significantly lower. The same ranking wasalso observed in non-grafted trees [sites 5 and 6 (Table la)]. Though P deficiencyhas not been identified in pistachio, several trees in this trial exhibited Pconcentrations of below 0.1%. This would be deficient for most other fruit andnut species (Beutel et al., 1972). The highest P concentrations observed (0.16-0.18%) would also be regarded as marginal for most species. The effect ofrootstock on leaf P concentration was significant only at the higher (though stillmarginal) levels of tissue P.
Calcium: Tissue Ca concentrations varied from 1.5 to 3.5% (Table la).Pistachio grafted on 'Integerrima' contained consistently higher Ca concentrationsthan did those with P. atlantica rootstock. UCBI was inconsistent in its responsebut was generally better than P. atlantica and often not as effective as P.
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1142 BROWN, ZHANG, AND FERGUSON
TABLE 1b: Micro-Nutrient Concentrations in Leaves of Grafted 'Kerman' and Non-Grafted Pistachio.
ElementManganese
(ppm)
Copper(ppm)
Zinc(ppm)
Boron(ppm)
Iron(ppm)
RootstockAtlanticaIntegerrimaPGIIUCBITerebinthus
AtlanticaIntegerrimaPGIIUCBITerebinthus
AtlanticaIntegerrimaPGIIUCBITerebinthus
AtlanticaIntegerrimaPGIIUCBITerebinthus
AtlanticaIntegerrimaPGIIUCBI.Terebinthus
Site1
37294129
13b6a9a9a
18b13a14a15a
101b71a100b68a
73616656
GraftedSite
243586983
7c5a6b6b
15b11a11a12a
124b63a88a82a
45464848
TreesSite
34647
4741
17b12a
10a12a
6364
6265
146162
139100
5153
5852
Site4
5157
5331
20b16a
10a12a
1313
145 4 *
261202
296105
6171
6452
Non-GraftedSite
539314230
14b7a8a8a
17b12a14a15a
110b77a
100a74 a
55585955
TreesSite
651545254
18b12a12a10a
15b12a13a11a
154163140100
62686562
All values are the means of 20 trees sampled in JulyNumbers with different letters differ significantly (P<0.05)* = probable contamination
integerrima or 'PGII' at increasing leaf Ca. The most significant effect of
rootstock was observed when leaf Ca was low (leaf Ca concentration <1.7%).
Differences in leaf Ca were most significant at marginal Ca sites. Thus, at site 1,
leaves of the scion 'Kerman' on P. integerrima had leaf Ca concentrations of 2.2%
compared with 1.3% on P. atlantica.
Copper: Leaves of 'Kerman1 grafted on P. atlantica had higher Cu con-
centrations than those on other rootstocks. This was observed at each site (Table
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NUTRIENT ACQUISITION BY PISTACHIO 1143
lb) and at all Cu levels. At site 2, several trees on PGII and P. integerrima
rootstock had visual signs of Cu deficiency. No Cu deficeincy was observed in
trees grown on P. atlantica. Leaves of trees grafted on P. integerrima were lowest
in tissue Cu concentration (sites 1 and 2). 'PGII', TJCBI1 and P. terebinthus were
intermediate in their response. The response in seedling rootstocks was similar,
with P. atlantica having higher leaf Cu than the other rootstocks at both sites. The
currently accepted critical level for Cu in pistachio is 4 to 6 ppm, using this criteria
no plant grafted on P. atlantica was deficient in Cu. Copper concentrations in P.
atlantica were as much as 2.5 times higher than in P. integerrima. The clear
benefits of P. atlantica warrant its consideration in areas of known Cu deficiency.
Zinc: Leaves of 'Kerman' grafted onto P. atlantica rootstock contained signi-
ficantly greater concentration of Zn than those grafted to other rootstocks (Table
lb). This effect was marked under both limiting and adequate Zn conditions
[critical leaf Zn levels are 15 to 18 ppm (Beutel et al., 1972)].
In a preliminary study conducted in 1990 scions on the rootstock P.
terebinthus had consistently high leaf Zn. This could not be verified in 1991 due to
Zn contamination from foliar sprays. Though the difference was small, P.
integerrima resulted in the lowest leaf Zn at 5 of 6 sites. Throughout, seedling
trees (sites 5 and 6) showed the same ranking in elemental concentrations as did
tree grafted on those rootstocks (Table lb). This indicates that the mechanism of
enhanced Zn uptake is root dependent and is expressed in the grafted tree. Five of
the six sites tested here had Zn levels below or near the critical value for pistachio,
demonstrating the widespread deficiency of this element.
Manganese: Differences in nutrient concentration between the different
rootstocks was small. No rootstock was significantly superior, though 'PGII' had
higher tissue Mn levels at two low Mn sites. Manganese deficiency is rarely seen
in pistachio and none of the levels reported here were below reported critical
values of 20 to 22 ppm.
Iron: No significant effect of rootstock on Fe nutrition was observed and all
concentrations appeared adequate.
Boron: As with Cu and Zn, the rootstock P. atlantica is superior at attaining B
from the soil (Table lb). Significantly, these differences were most marked at the
lower B concentrations (mean B concentration <100 ppm). At only one site, with
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1144 BROWN, ZHANG, AND FERGUSON
adequate B [150 ppm B (Brown et al., 1992)], did rootstock significantly
influence leaf B concnetrations (site 4). Leaf B concentrations were highest in P.
atlantica, followed by 'PGII' while P. integerrima and 'UCBI' consistently
resulted in the lowest leaf B.
Correlation Analysis: Correlation analysis was performed on the pooled data
to determine if high leaf level of one nutrient is correlated with leaf levels of other
nutrients. A positive correlation between nutrients would suggest that a single trait
(probably related to root characteristics) was responsible for the increase in leaf
nutrient concentration. There was a close positive correlation between leaf Cu
concentration and leaf B (r2 = 0.6, P>0.0 1). Rootstocks efficient in enhancing
leaf B concentrations were also effective at enhancing leaf Cu concentrations. Leaf
P concentrations were positively correlated with leaf Mg (r2 = 0.75, P>0.01), but
not Ca, Mn, or Fe uptake. There was no significant correlation between any other
elements.
DISCUSSION
Precise critical nutrient values for pistachio have not been established, and in
California, we have not observed P, Mg, Ca, Fe, or Mn deficiency in field
situations. Given these limitations it is difficult to interpret the significance of
rootstock effects on leaf P, Mg, Ca, Fe or Mn concentrations. The value of this
information may become apparent later. On the other hand, deficiencies of Zn, Cu,
and B are widespread. For Cu and Zn, deficiencies are difficult to correct since
soil conditions often limit Cu, Zn availability from fertilizers and foliar sprays are
of only limited value. The following discussion will be limited to these elements of
known practical significance.
Leaf nutrient concentrations in non-grafted rootstock trees followed the same
relative ranking as grafted trees on these same rootstocks. This suggests that
factors influencing nutrient acquisition by the rootstock are expressed in the
grafted plant. This is not always the case and there are several instances where
nutrient efficiency of the non-grafted rootstock is not expressed in the scion
(Thomas and White, 1950; Wutscher, 1989). The effectiveness of pistachio
rootstock choice at influencing leaf nutrient concentration in both grafted and
non-grafted situations, coupled with the observation that these effects occur in a
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NUTRIENT ACQUISITION BY PISTACHIO 1145
variety of soils and plant ages, suggests that rootstock choice can be a useful
management tool in nutrient poor soils.
Pistacia atlantica is the most effective rootstock in terms of enhancing leaf
concentrations of the major limiting nutrients (Cu, B, and Zn). Significantly, the
hybrid rootstocks derived from crosses between P. atlantica and P. integerrima
used in this comparison (i.e., 'PGII' and TJCBI') resembled the P. integeririma
parent, in terms of nutrient characteristics, more than they resembled P. atlantica.
Currently, all hybrid seed available in California is generated from no more than
three male and three female trees. Given this very limited parentage, and the
variation in leaf nutrient concentration observed within P. atlantica (data not
shown), it is not surprising that the progeny of these limited crosses (i.e., PGII
and UCBI) did not exhibit the relative nutrient efficiency of the P. atlantica parent.
A more extensive crossing program may result in the incorporation of Cu, Zn, and
B uptake efficiency in future hybrid rootstocks.
The mechanisms influencing the differential nutrient uptake by the five
pistachio rootstocks are not known. Gross differences in root growth, degree of
branching or assimilate partitioning would be expected to result in improved
nutrient concentrations (or growth) for most of the major elements. This was not
observed in this study. Typically, rootstock choice resulted in the enhancement of
only a few plant essential elements. Scions grafted on Pistacia atlantica for
instance, had higher leaf Zn, Cu, and B concentrations but depressed Ca and Mg.
In contrast, P. integerrima was relatively more effective at increasing leaf Ca than
was P. atlantica, but was poor at providing Cu, Zn, or B to the scion. Thus gross
differences in root length or density cannot adequately explain the observed differ-
ences. Similarly, these results cannot be explained by differences in crop yield or
transpiration.
The supply of nutrients to roots is dependent on three processes, mass flow,
diffusion, and root interception. An increase in root size and soil volume would
enhance uptake of those nutrients supplied by root interception and diffusion
(Barber and Sillerbush, 1982). Thus an increase in root density would enhance Cu
and Zn uptake but would not affect B uptake (mainly supplied by mass flow). In
addition, specific mechanisms may exist for Cu and Zn uptake similar to those
exhibited for Fe uptake (Zhang et al., 1991). Nutrient efficiency may also involve
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1146 BROWN, ZHANG, AND FERGUSON
mycorrhizae, or any of the variety of nutrient mobilizing strategies identified in
other species (see discussion in Marschner, 1986). The ability of P. atlantica to
efficiently acquire Cu and Zn may suggest the production of mobilizing chemicals
(chelators and reductants) or root induced changes in pH. The lack of this
rootstock effect on Fe or Mn concentrations, however, would suggest the
operation of a specific mobilization mechanism, rather than a more general
response such as pH reduction at the root surface. Enhanced uptake of B by P.
atlantica cannot be easily explained by our current knowledge of B uptake and
movement in the soil.
The correlation between B and Cu suggests that there is a common (or
genetically linked) mechanism for acquisition of these elements. Significantly,
'Kerman' grafted onto P. atlantica also had the highest leaf P concentrations
though the correlation between leaf P and Cu or B was not significant at the 5%
level (r2 = 0.56 and 0.61, p<0.08 and 0.06, respectively). However, there was
little or no correlation between leaf Zn concentrations and B or Cu concentrations.
This suggests that the uptake of P, B, and Cu is interrelated, but that the uptake of
Zn involves a distinct process. The effect of rootstock on leaf P, B, and Cu may
be due to mycorrhizha since there is evidence to suggest that P, Cu, and perhaps B
uptake can all be enhanced by mycorrhizal association with the roots (Marschner,
1986). We tested this hypothesis by sampling roots collected from representative
rootstocks at site 2. In a series of 20 root samples we isolated mycorrhizal roots
from P. atlantica but could not isolate mycorrhizae from any other rootstock
species (unpublished data). The observed differences in nutrient efficiency may be
due to differential mycorrhizal infection of the various root- stocks. If mycorrhizal
infection is a significant factor in the relative nutrient efficiencies of pistachio
rootstocks then selection and inoculation with appropriate mycorrhiza may be
beneficial. Further research is required.
Pistachio rootstocks are chosen for a number of reasons including Verticillium
resistance, cold hardiness, and uniformity of growth. This research demonstrates
that P. atlantica has some useful nutritional traits, however, P. atlantica is known
to be susceptible to root fungal pathogens and is thought to be less uniform in its
yield. Nevertheless, there are many regions within California in which Cu and Zn
deficiency is severe and root pathogens are limited. In these regions, P. atlantica
may be the best rootstock choice.
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NUTRIENT ACQUISITION BY PISTACHIO 1147
CONCLUSION
It is recommended that the nutritional characteristics of pistachio rootstocks be
considered when planting in areas with known nutritional deficiencies. This is
particularly significant for Cu, Zn, and B for which deficiencies do occur in the
field and amelioration is difficult and expensive. Frequent foliar or soil appli-
cations, including expensive chelated material, are both labor intensive and costly.
The availability of nutritionally efficient rootstocks and the ongoing need for Cu,
B, and Zn enhancement in pistachio suggests that nutrient uptake characteristics
should be included in future pistachio breeding programs.
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Ashworth, J. 1985. Verticillium resistant rootstock research, pp. 54-56. AnnualReport of the Californian Pistachio Industry. Fresno, CA.
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Crane, J.C. and B.T. Iwakiri. 1987. Pistachio yield and quality as affected byrootstock, pp. 86-88. Annual Report of the Californian Pistachio Industry.Fresno, CA.
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1148 BROWN, ZHANG, AND FERGUSON
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