Trees (2014) 28:879–890 DOI 10.1007/s00468-014-1001-6
ORIGINAL PAPER
The effects of temperature and drought on autumnal senescence and leaf shed in apple under warm, east mediterranean climate Shaul Naschitz • Amos Naor • Shmuel Wolf Eliezer E. Goldschmidt
•
Received: 20 June 2013 / Revised: 1 January 2014 / Accepted: 25 February 2014 / Published online: 15 March 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Key message Autumnal senescence of apple in a warm climate corresponds to accumulated degree-days beneath 22 °C. Summer drought delays senescence and enables replenishment of carbohydrate reserves. Recovery of the root system plays a key role. Abstract Autumnal senescence of apple (Malus domestica Borkh.), a deciduous, temperate climate species, is triggered by a rather abrupt temperature drop, down to the lower teens. Under the warmer, east Mediterranean climate of northern Israel, the temperature drop is gradual and much more moderate. Another characteristic of this climate is the complete lack of precipitation during summer. The aim of the present study was to elucidate the effects of summer drought on seasonal leaf senescence in a warm autumn. We hypothesized that summer drought delays senescence due to an increased demand for carbohydrates during autumn. The advent of autumnal senescence was followed for 3 years (2009–2011) on trees exposed to various levels of drought. Total canopy green area (effective leaf area, ELA) and hue angle were estimated
periodically by means of image analysis, as a measure of leaf drop and autumnal color change. Photosynthesis, midday stem water potential, and roots’ non-structural carbohydrate contents were measured on several occasions. The time course of leaf drop followed the decline in air and soil temperatures. The rate of decline in ELA closely corresponded to accumulated degree-days beneath 22 °C in the soil, a much higher temperature threshold than previously reported for apple. Drought stress during the summer delayed leaf senescence even further, when compared with well-irrigated trees. Leaves maintained their photosynthetic functionality throughout autumn, until late December. The delayed senescence enabled replenishment of root carbohydrate reserves, which is critical for next year’s growth and fruiting. The eco-physiological significance of the findings is discussed. Keywords Autumnal senescence Drought Malus domestica Non-structural carbohydrates Root system
Introduction Communicated by K. Masaka.
Electronic supplementary material The online version of this article (doi:10.1007/s00468-014-1001-6) contains supplementary material, which is available to authorized users. S. Naschitz (&) S. Wolf E. E. Goldschmidt The Robert H. Smith Faculty of Agriculture, Food and Environment, Institute of Plant Sciences and Genetics in Agriculture, The Hebrew University of Jerusalem, P.O.Box 12, 76100 Rehovot, Israel e-mail:
[email protected] A. Naor The Golan Research Institute, P.O.Box 97, 12900 Katzrin, Israel
The transition from summer to autumn marks a fundamental shift in the physiology of deciduous trees. Growth ceases in favor of retention of organic and mineral resources within perennial organs (Tromp 1983). Cold hardiness builds up while leaves senesce and abscise. This is a committed, irreversible process. The tree must time it early enough to avoid low temperature damage, but late enough in order to fix the carbon required for bloom and leaf expansion in the following spring. The important role of short photoperiods as the signal inducing autumnal senescence has been demonstrated in a variety of temperate zone woody plants (e.g. Nitsch 1957; Heide 1974). An
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exception to the short day control of autumnal senescence in temperate trees and shrubs has been reported for apple (Malus domestica Borkh.) and some other woody genera of the Rosaceae (Nitsch 1957; Jonkers 1980; Heide 2011). Heide and Prestrud (2005) demonstrated that growth cessation, leaf senescence and fall and bud scale formation in several apple rootstocks are promoted by exposure of the plants to temperatures lower than 12 °C regardless of the photoperiod. Freezing temperatures induced rapid leaf drop (Tartachnyk and Blanke 2004) and deepen dormancy (Cook et al. 2005). Apart from temperature, autumnal leaf senescence is regulated by the existence of active sinks for carbohydrates and nutrients in the plant. De-fruiting of potted apple trees in October resulted in a sharp decline in net photosynthesis and in water use efficiency (Wibbe and Blanke 1992). Conversely, delaying fruit harvest of apple postponed the onset of leaf senescence by a few weeks even at low temperatures (Tartachnyk and Blanke 2004). In deciduous trees, carbohydrate and nitrogen reserves play a crucial role in the emergence and growth of new organs in the following spring. The entire energetic requirements of the tree rely on stored carbohydrates until sufficient leaf area has developed to support the newly established tissues (Loescher et al. 1990; Teng et al. 1999). In woody perennials, the root system is the major storage organ, for both carbohydrates and nitrogen (Tromp 1983). Towards the end of summer and during autumn roots become the highest priority sink and accumulate large amounts of carbohydrates (Tromp 1983; Kosola et al. 2002). The timing of leaf senescence in the autumn may determine the plant’s potential to recover its carbohydrate reserve pool prior to winter dormancy and thus the availability of resources to support bloom and fruit set in the following year, as was demonstrated in pecan (Sparks 1978). Apple is traditionally grown in regions characterized by temperate climates with ample water supply, where steep declines in temperature and solar irradiation during autumn limits photosynthesis and induces rapid leaf drop. However, when temperature decreases slowly over a long period as typical to the Mediterranean basin the induction of dormancy cannot be easily related to changes in atmospheric conditions. Trying to define the environmental factors that promote senescence at low latitudes has caused some confusion (Cook and Jacobs 2000). Another characteristic of the Mediterranean climate is lack of precipitation in the period between May and October, resulting in rather intense summer drought (Mooney et al. 1974) which may interfere with photosynthetic activity and carbohydrate budget of the tree. The effect of summer drought on autumnal senescence has not been investigated. We hypothesized that drought stress during summer postpones leaf senescence in response to the strong demand
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for carbohydrates by the recovering root system. We further hypothesized that the mild Mediterranean autumn enables extended photosynthetic activity and carbohydrate storage in trees after fruit harvest while temperature control over leaf senescence is rather weak. Overwintering carbohydrate stores are critical for renewal of growth in spring. A variety of water supply regimes were utilized to test this hypothesis. While the study was conducted in a partially controlled environment, the irrigation regimes employed represented natural soil water availability in a range of climate zones. Background information on the dynamics of autumnal climate under Mediterranean conditions had to be assembled and analyzed in order to form the basis for the experimental study.
Materials and methods Experimental site The experimental plot was situated in a commercial apple orchard in northern Israel, 33.0N 35.3E at an altitude of 670 m above sea level. During June through September, average daily maximum and minimum temperatures are 31 and 19 °C, respectively, with little variation. Precipitation does not occur during the summer and practically all the water requirement of the tree is supplied artificially, starting in early May and ending in early November. Climatic averages and hourly weather data for the experimental plot were obtained from an automatic weather station (Campbell Scientific, UT, USA) located on the site. Plant material The study was carried out on healthy, mature Malus domestica ‘Golden Delicious’ trees grafted on Malus domestica ‘MM106’ rootstock. Trees were 17 years old in 2009 and spaced 2.5 m 9 4.5 m. Orchard rows formed a thin hedgerow approximately 3.5 m in height. Irrigation trial Four water supply regimes were examined: 1, 2, 4 or 7 mm day-1 all applied invariably between early June and September in 2009 and 2010. Each treatment was applied to eight trees set in two blocks. Irrigation blocks were surrounded by border trees and rows. The same treatment was applied to each tree in 2009 and 2010. Immediately after fruit harvest the highest irrigation rate was reduced to 4 mm day-1 to avoid runoff. Water was supplied daily using a drip system. An effort was made to minimize water percolation beneath the root zone by restricting continuous water supply to 1 mm pulses. In 2011, all the trees were
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Fig. 1 Processing of tree photographs: mosaicing and separation of green squares to estimate effective leaf area (ELA)
irrigated according to commercial practice, which is similar to the 7 mm day-1 treatment. All trees were grown according to commercial practice until early June, except that irrigation and chemical fruit thinning were not applied. In 2009, differential irrigation was initiated on 5 June 2009, 48 days after full bloom (DAFB). Trees were harvested on 13 September 2009. Irrigation ceased by the first autumn rainfall, which occurred on 1 November 2009. In 2010, differential irrigation was initiated on 20 May 2010, 48 DAFB. Trees were harvested on 31 August 2010. Irrigation ceased by the first autumn rainfall, which occurred on 10 December, 2010. In 2011, all trees were fully irrigated throughout the growing season, starting on 18 May and ending by early November. Estimation of effective leaf area (ELA) In 2009–2011, the trees were occasionally photographed between mid-October and late December. Photographs were taken laterally, at approximately 2 m above ground and from a distance of approximately 3.5 m. A 7 9 7 cm sheet of paper, similar in area to a typical leaf, was attached to each tree at 2 m above ground for pixel calibration. Photographs were then run through a mosaicing procedure
using a square size equivalent to 4 9 4 cm (Fig. 1). This procedure was performed in order to differentiate leaves on the measured tree from those on trees in the distance. It was assumed that mosaic squares depicting foliage of a nearby tree would appear more saturated (with higher chroma) than squares depicting foliage of a distant tree (Fig. 1). Green mosaic squares (hue angle between 55° and 141°; chroma levels above 105) were counted in the photographs, and their total equivalent area was calculated and multiplied by a factor of 2.5 to represent both sides of the tree and integrate the changing solar angle (Campbell and Norman 1998). The resulting area is referred to as effective leaf area (ELA), which is the portion of a tree’s green leaf area exposed to direct solar irradiation during at least a part of the day. To track changes in leaf color, the mean hue angle of all pixels with hue angle between 30° and 141° and chroma level above 105 was computed for each photograph. All image processing and analyses were performed using LeadTools 14.0 software (Lead Technologies, Charlotte, NC, USA). Predicting temperature thresholds for leaf senescence Air (2 m above ground) and soil (20 cm below ground level) temperature data recorded between early October and
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late December of all 3 years were used for the analysis. Accumulated degree-days (ADD) below various base temperatures, iterated at 1 °C intervals between 12 and 24 °C were computed. The mean relative effective leaf area (RELA—defined as the ratio between ELA on measuring date and the full-canopy ELA in the respective year) was plotted against ADD at different base temperatures. Each data point represented the average RELA of eight trees. The temperature threshold had to satisfy two criteria: a uniform response curve of RELA to ADD between years and the best fit of a model which relied on the multi-year data. Hence, two statistical procedures were employed in order to determine the temperature threshold for leaf senescence: (a)
(b)
It was assumed that the temperature threshold of leaf senescence is physiological in nature and does not vary between years. Thus the response of RELA to ADD was expected to manifest the highest degree of convergence among years when ADD was based on the temperature threshold. RELA was plotted against ADD with ‘year’ serving as a main effect. A separate linear regression was obtained for each year. The F ratio for ‘year’ (defined as the variance of RELA between years divided by its variance within years) was selected as a measure of divergence where higher F ratios denoted a higher degree of divergence between curves. The corresponding P values were used to test whether the responses of RELA to ADD in different years were significantly different. The root of mean square errors (RMSE) and Akaike’s information criterion (AIC) were used to compare the efficiency of the entire model at various base temperatures where smaller values represented better fits (Snyder et al. 1999; Miranda et al. 2013). RELA was plotted against ADD using the combined data of all 3 years. The analysis was performed by the generalized linear model (Nelder and Wedderburn 1972). All observations where RELA was larger than 0.1 were included. This model obtained a single declining curve for each base temperature with Y values ranging between 0 and 1. It was assumed that the maximum likelihood for the model would be obtained when base temperature was closest to the threshold. AIC was used to compare different base temperatures. By definition, the intercept of the response when using the threshold temperature as base for ADD computation would be 1, meaning that ELA begins to decline concomitantly with the beginning of accumulation of degree-days (Fig. 2). In a secondary procedure, the intercept was plotted against base temperature to determine the approximate temperature at which it met the value 1.
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Fig. 2 A schematic description of the change in normalized surviving effective leaf area (ELA) as affected by accumulated degree-days beneath a given temperature. If the specified temperature is lower than the true threshold, ELA begins to decline prior to the accumulation of degree-days, resulting in a regression with an intercept smaller than 1; if the specified temperature is higher than the true threshold, degree-days accumulation precedes the decline in ELA, resulting in a regression with an intercept greater than 1; if the specified threshold matches the true threshold, the beginning of ELA decline coincides with the beginning of degree-day accumulation. In this case, the intercept of the regression is expected to equal 1 Fig. 3 Weather data collected during autumn in 2009, 2010 and c 2011: minimum air temperature (a), maximum air temperature (b), daily global radiation (c), mean soil temperature (d), accumulated time of air temperature \12 °C (e), accumulated time of soil temperature \20 °C (f) and accumulated precipitation (g)
The analyses were restricted to fully irrigated trees in order to eliminate possible effects of drought stress on senescence thresholds. Photosynthesis measurements Maximum assimilation rate (Pn) and stomatal conductance (Gs) were measured on 20 October, 4 November, 25 November and 23 December, 2010. Measurements were performed to intact leaves between 10 a.m. and noon using a CIRAS-2 gas exchange analyzer (PP Systems, Amesbury, MS, USA). Three green, sun-exposed leaves on each tree were selected for the measurements. The measurement conditions applied were ambient temperature (ranging between 18 and 28 °C, depending on date), 390 ppm CO2 and 1,200 lmol m-2 s-1 PAR. Non-structural carbohydrates analysis Branch wood sections and roots were sampled from all trees on 8 February 2010, at full dormancy, for nonstructural carbohydrate (NSC) analysis. Branch sections measuring 8–10 mm in diameter and approximately 15 mm in length from mature wood and root sections
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measuring approximately 5 mm in diameter and 50 mm in length were used. Plant material was dry-heated in an oven to 90 °C for 90 min to eliminate all enzymatic activity (Scha¨del et al. 2009). Thereafter the samples were cut to 2-mm-thick slices and dried at 65 °C for an additional 36 h before storage at -18 °C until analysis. The material was then grinded to a fine powder. Starch content was determined according to the method described by Li et al. (2003) and Naschitz et al. (2010). Samples were repeatedly rinsed with ethanol to remove all soluble sugars and reacted with the enzyme amyloglucosidase to hydrolyze the starch. Thereafter soluble sugar content was determined spectrophotometrically. Sucrose, glucose, fructose and sorbitol contents were determined by HPLC following the method described by Olesinski et al. (1996). All carbohydrate concentrations were measured on a dry weight (DW) basis. Midday stem water potential measurements Midday stem water potential (SWP) was measured on 23 September 2009 and on 11 October 2010. Two intact leaves from the shaded portion of the canopy of each tree were sealed with plastic bags wrapped in aluminum foil pre noon, allowing them to reach equilibrium with the stem for at least 90 min; then they were removed by a sharp cut through their petioles, covered with a plastic bag and immediately inserted in a pressure chamber (‘Arimad II’, Kfar Haruv, Israel) where pressure was gradually increased using compressed nitrogen. Chamber pressure was recorded at the stage when a droplet formed at the cut end of the petiole. Statistical analysis Results were analyzed using the SPSS 19 software (IBM, Armonk, NY, USA). Linear regressions and ANOVA were used to compare treatments where applicable. The statistical procedure used for evaluating temperature thresholds of leaf senescence is described in the corresponding section.
Results Course of autumnal changes The 2009–2011 weather data revealed considerable yearto-year fluctuations in temperature and precipitation (Fig. 3), typical to the dry, Mediterranean climate of northern Israel. The average autumn (October–November– December) maximum temperature ranged between 23.1 °C in the warmest year (2010) and 18.2 °C in the coolest
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Fig. 4 Progressive changes of effective leaf area (ELA) (a) and leaf color (b) in three consecutive years in fully irrigated mature apple trees cv. ‘Golden Delicious’. Each value represents the average of eight trees. Vertical bars represent standard errors
(2011). Accumulated precipitation until the end of November ranged between 153 mm in the wettest year (2009) and 47 mm in the driest (2010). The kinetics of leaf fall in well-irrigated trees represented by ELA (Fig. 4a) shows an almost linear decline over time. Leaf color curves (Fig. 4b) slightly lagged behind the reduction in ELA. The readings of hue angle from photographs reflected the chlorophyll content of representative leaves (data not shown). The coolest and warmest years among the three revealed the earliest and latest changes in ELA, respectively. Declines of both soil and air temperatures promoted leaf senescence (P \ 0.0001, respectively). The response of RELA to air ADD varied between years (P [ 0.05) except when ADD was computed with 12 °C or 13 °C as base temperatures (Fig. 5a). However, those base temperatures did not align with the lowest AIC or RMSE (Fig. 5b, c, respectively), suggesting that in our conditions air temperature cannot be used as a reliable predictor of the timing or rate of autumnal leaf senescence. Conversely, the response of RELA to soil ADD did not differ between years throughout the temperature range tested. The predicted threshold soil temperature for leaf senescence in fully irrigated trees was 22 °C (Table 1), where AIC reached a minimum (Fig. 6a) and the intercept of the model crossed the value of 1 (Fig. 6b). The model
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885 Table 1 Predictions of air and soil temperature thresholds for autumnal leaf senescence Model
Separate linear regressions
Generalized linear model for all years
Criterion
Predicted temperature threshold Soil (°C)
Air
Minimum F ratio (year)
22
12 °C
Minimum AIC Minimum RMSE (model)
23 22
22 °C 23 °C
Minimum AIC
22
NA
Intercept crossing 1
22.0
NA
The mean fraction of surviving effective leaf area of eight fully irrigated trees was plotted against accumulated degree-days beneath various thresholds for three consecutive autumns (2009–2011). Two models were generated: (a) a per-year linear regression and (b) a combined generalized linear model for all years. Various criteria were used to evaluate the best temperature thresholds: minimum F ratio for ‘year’ (model a), minimum root of mean square errors (RMSE— model a), minimum Akaike’s information criterion (AIC—models a, b) and the base temperature for which the intersect of the regression crosses 1 (model b)
Fig. 5 Statistics of a per-year linear regression of the effect of accumulated degree-days beneath a specified temperature on the proportion of surviving effective leaf area (ELA). The model was applied to ELA values obtained for fully irrigated apple cv. Golden delicious trees based on air and soil temperature data. The F ratio for the year variable (a), Akaike’s information criterion (AIC, b) and the root of mean square error (RMSE, c) are presented. Each data point represents the mean fraction of surviving ELA of eight fully irrigated trees as compared to their ELA in early October. Significant F ratios (P \ 0.05) are marked with asterisk
predicted that 254 ± 14 (SE) degree-days beneath 22 °C in the soil are required for the completion of leaf shed. Drought and water supply The level of water supply during summer affected leaf fall; drier regimes delayed the decline in ELA for up to several weeks in 2009 (Fig. 7a), but not in 2010 (Fig. 7b). Autumnal photosynthetic activity in 2010 appeared to be limited, however, by drought. Figure 8 shows that drought-
stressed trees had very low photosynthetic activity in October, which then gradually increased, presumably due to improvement of the water status as air temperature (Fig. 3) and vapor pressure deficit declined. Fully irrigated trees, on the other hand, revealed high photosynthetic activity which gradually declined starting at the end of October (Fig. 8). Early, sporadic rain events which occurred both in 2009 (late September—41 mm) and in 2010 (early October— 40 mm) revealed that despite a substantial amount of rainfall available to all trees, differences in SWP between previously water-deficient and well-irrigated trees persisted (Fig. 9): previously drought-stressed trees failed to take advantage of the abrupt increase in soil moisture to the same extent non-stressed trees did. Accumulation of carbohydrates in overwintering organs The 2009–2010 mid-winter non-structural carbohydrate content of coarse roots and branch wood is presented in Table 2, for two of the water supply treatments. Roots accumulated much higher concentrations of total NSC and in particular, starch, than branch wood. Mid-winter root starch seems to reflect differences in the onset of autumnal senescence; higher root starch content in February was related to higher ELA during mid-October (Fig. 10). Mean starch content in roots of water-deficient trees exceeded 250 mg g-1 DW, a much higher value than previously reported (Greer et al. 2002). In the winter of 2010–2011, average
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Fig. 6 Statistics of a multi-year generalized linear model for the effect of accumulated degree-days beneath a specified temperature on the proportion of surviving effective leaf area (ELA). The model was applied to ELA values obtained for fully irrigated apple cv. Golden delicious trees based on air and soil temperature data. Akaike’s information criterion (AIC, a) and the intercept of the regression at different temperature thresholds (b) are presented. Each data point represents the mean fraction of surviving ELA of eight fully irrigated trees as compared to their ELA in early October. Vertical lines represent standard errors of the intercept
root carbohydrate contents were around 180 mg g-1 DW and did not differ among water supply treatments, reflecting the uniform advent of leaf shed (Fig. 7b).
Discussion Three years of autumnal follow-up demonstrated the slow, gradual onset of leaf senescence under the warm, east Mediterranean climate conditions (Fig. 4). Although the follow-up was conducted with trees irrigated to various proportions of their water requirements, the drought-stressed, 1 mm day-1 irrigation treatment (Fig. 7) might be representative of the natural growth and autumnal senescence processes in this climate. The statistical analysis indicated that soil temperatures below 22 °C are sufficient to set the senescence process into motion under these conditions (Table 1). While temperatures above 21 °C have been reported to interfere with winter chilling in some agricultural crops of the Rosaceae
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Fig. 7 Progressive change in effective leaf area (ELA) in mature cv. ‘Golden Delicious’ apple trees subject to different water supply regimes in 2009 (a) and 2010 (b). Each value represents the average of eight trees. Vertical bars represent standard errors
family in warm climates (e.g. Gilreath and Buchanan 1981; Shaltout and Unrath 1983), this finding is in an apparent contrast with a 12 °C threshold reported for apple under north European climate by Heide and Prestrud (2005). We have presently no clear explanation for this eco-physiological difference, but the involvement of an epigenetic adaptation mechanism cannot be ruled out (Yakovlev et al. 2010; Bra¨utigam et al. 2013). Our results indicate that autumnal senescence is more tightly related to temperature in the rhizosphere than to air temperature (Figs. 5, 6). It is possible that this result merely reflects the more gradual, less erratic decline in soil temperature (Fig. 3) which behaves in a similar manner to the gradual yellowing and shed of foliage. However, the differences in SWP between trees exposed to different water supply regimes, as recorded shortly after two early rain events (Fig. 9), the effects of summer drought on ELA decline rate (Fig. 7) and the proximity of the threshold soil temperature found to levels at which root growth begins to decline (Pregitzer et al. 2000) imply that roots play a central role in the advent of autumnal senescence. The hypothesis that formed the basis for this study was that summer drought delays senescence due to increased demand for carbohydrate during autumn. The apparent contribution of summer drought to extension of the growing season through late autumn in 2009 (Fig. 7a) supports our hypothesis. The autumn of 2009 was characterized by
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Fig. 8 Mean Pn for drought-stressed and fully irrigated trees during the autumn of 2010. Each value represents the average of eight trees. Vertical bars represent standard errors
Fig. 9 Midday stem water potential (SWP) as measured in trees subject to different water supply treatments, 72 h after early, isolated rain events which occurred on 20 September 2009 and 8 October 2010. Each value represents the average of eight trees. Vertical bars represent standard errors. P(year) [ 0.1; P(irrigation) \ 0.001. Different letters denote significantly different treatments
cooler temperatures than the ones that prevailed in 2010, inducing leaf senescence by late October as opposed to mid-November in 2010 (Fig. 3d) and resulting in *40 days of un-interrupted growth after harvest as
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opposed to *75 days in 2010. We speculate that the delay of senescence is mediated by the persistence of root growth throughout autumn in previously stressed trees. In 2010, higher post-harvest soil temperatures presumably allowed roots of drought-affected trees to fully recover prior to induction of leaf senescence. This may account for the minimal effect of drought on the timing of leaf shed (Fig. 7b). Despite the longer growing season, roots accumulated less starch in 2010 than in 2009 (Fig. 10). Root starch concentration is affected by ELA, but it is also affected by the photosynthetic activity (which in turn depends on temperature, light and soil moisture), by the internal partitioning of assimilates between growth and storage, and by starch already accumulated during summer. It is hypothesized that the much higher soil temperatures in the autumn of 2010 (Fig. 3d) promoted root growth at the expense of storage (Tromp 1983). The deficit in root mass at fruit harvest might have been greater in 2010 than in 2009, following an unusually hot summer (Yao et al. 2009). During the summer, shoot growth and then fruit growth are prioritized over root elongation and renewal (Lakso et al. 1999; Marsal et al. 2008), resulting in an increased sensitivity of the root system to adverse growing conditions. Consequently, trees exposed to drought in controlled conditions suffered a dramatic reduction to their root mass while other organs gained dry matter (Buwalda and Lenz 1992). Another study demonstrated a sharp increase in fine root mortality concomitant with a reduction in root elongation rate as a result of drought (Yao et al. 2009). Roots may recover in the autumn after de-fruiting had occurred (Tromp 1983; Eissenstat et al. 2000; Kosola et al. 2002; Comas et al. 2010). During the long, warm post-harvest period which is characteristic to the Mediterranean climate, quite intense
Fig. 10 The relation between starch concentration in coarse roots sampled on 8 February 2010 and effective leaf area (ELA) of the same tree as estimated on 15 October 2009. Each value represents one tree (r2 = 0.38; P \ 0.001)
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Table 2 Concentrations of non-structural carbohydrates (NSC) in coarse roots and in branch wood of mature apple trees cv. ‘Golden Delicious’ at 8 February 2010 Tissue
Irrigation rate (mm day-1)
Starch
Sucrose
Glucose
Fructose
Sorbitol
Total NSC
Coarse roots
2
269.1 ± 16.4
0.96 ± 0.11
7.65 ± 0.43
8.40 ± 0.46
18.0 ± 1.0
304.1 ± 18.4
7
176.9 ± 11.9
0.79 ± 0.12
7.46 ± 0.72
8.73 ± 0.70
17.7 ± 1.2
211.6 ± 14.6
2
37.9 ± 5.2
4.66 ± 0.95
6.94 ± 0.98
8.62 ± 1.10
27.4 ± 2.2
85.5 ± 10.4
7
33.7 ± 5.5
4.48 ± 0.77
7.78 ± 0.66
9.81 ± 0.83
24.9 ± 1.9
79.7 ± 9.7
Branch wood
Values are in mg g-1 DW ± SE
solar radiation and relatively long photoperiods allow for the production of much more assimilates than in a colder climate, given adequate soil moisture and leaf area (Figs. 7, 8). A drought stress-induced delay of senescence may increase the overall production of assimilates even further (Fig. 10). Those resources are utilized for the recovery of the root system before the dormant season (Yao et al. 2009). Furthermore, the large pool of carbohydrates stored in overwintering tissues, primarily roots (Table 2; Naschitz et al. 2010), supports growth and development early in the following growing season (Sparks 1978; Tromp 1983; Greer et al. 2002). Thus, a warm autumn might be advantageous for the survival of the tree and compensate for periods of drought stress and low photosynthetic competence during summer. Assuming that recovery of the root system plays a central role in the onset of autumnal senescence it remains to be understood how the roots communicate with the aerial, above ground tree organs. Hormonal signals might be the answer, as outlined in Fig. 11. Growing roots are known to produce cytokinins and gibberellins which reach the canopy via the xylem, thereby preventing the onset of senescence (Greer et al. 2006; Malcolm et al. 2007; Kittikorn et al. 2010). Once the root system reaches a certain volume fine roots cease growing, the hormonal signal weakens and senescence begins. Root growth may also be interrupted by a drop in soil temperature beneath a physiological threshold (Pregitzer et al. 2000). Carbohydrate partitioning in the root system itself is controlled by soil temperature; whereas high temperatures promote root growth, lower temperatures, which prevail towards late autumn, inhibit growth and promote storage (Tromp 1983); hence the higher starch content found in roots of late-senescing trees (Fig. 10). In conclusion, the control of autumnal senescence by temperature seems rather flexible; the presence of active sinks such as fruit (Tartachnyk and Blanke 2004) or, under our conditions, the recovering root system modifies it and allows for further extension of the growing season until late December (Figs. 7, 8). The difference in the effects of drought on the course of leaf senescence between cooler
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Fig. 11 A schematic model describing the presumed role of the root system in the control of autumnal senescence. The model assumes deficient root mass at the time of fruit harvest as a consequence of competition aggravated by drought. The autumnal flow of carbohydrates enables recovery of the root system; the growing roots export gibberellins (GA) and cytokinins (CK) to the canopy, thereby delaying leaf senescence and extending photosynthetic competence. Soil moisture, leaf area, air temperature and solar irradiation dictate photosynthetic rate while soil temperature determines the partitioning of carbon between root growth and storage. This ongoing positive feedback cycle comes to an end when soil temperature drops to a level at which root growth stops altogether or when the root system reaches adequate mass/volume
(Fig. 7a) and warmer (Fig. 7b) autumns suggests that the onset of autumnal senescence depends on the synchronization of declines in sink activity and temperature. Those processes are closely related in cooler climates where growth is directly inhibited by low autumn temperatures, but less so in the mild Mediterranean autumn. It seems that previous exposure to drought per se does not change the temperature threshold of autumnal senescence. Instead it extends the period required for the recovery of the root system, which in turn sets a second condition for the onset of senescence. Only when both conditions (low
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temperature and adequate root recovery) are satisfied leaf senescence begins. All in all, the present research addressed one aspect of the behavior of apple trees under warm, east Mediterranean conditions. Further study of the apple survival under suboptimal climates is highly desirable. In this context, the behavior of roots deserves particular attention. Acknowledgments We gratefully acknowledge the financial support by the Chief Scientist of the Israeli Ministry of Agriculture. We thank Jose Gruenzweig and Joseph Riov for reviewing the manuscript and Or Shapira, Carmel Biederman, Harel Agra, Moshe Agiv and Ami Kauffmann for their technical assistance. Conflict of interest of interest.
The authors declare that they have no conflict
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