The effect of summer shading on flower bud ... - Springer Link

Cent. Eur. J. Biol. • 8(1) • 2013 • 54-63 DOI: 10.2478/s11535-012-0109-1

Central European Journal of Biology

The effect of summer shading on flower bud morphogenesis in apricot (Prunus armeniaca L.) Research Article

Susanna Bartolini1,*, Raffaella Viti2, Lucia Andreini1 Sant’Anna School of Advanced Studies, Life Science Institute, 56127 Pisa, Italy

1

Department of Trees Science, Entomology and Plant Pathology, ‘G. Scaramuzzi’, University of Pisa, 56124 Pisa, Italy

2

Received 27 July 2012; Accepted 20 September 2012

Abstract: The aim of this investigation was to assess whether imposed summer shading treatments in apricot (Prunus armeniaca L.) can affect the main phenological phases related to the floral morphogenesis (floral differentiation, xylogenesis), flower bud growth and quality in terms of bud capacity to set fruit. Experimental trials were carried out on fully-grown trees of ‘San Castrese’ and ‘Stark Early Orange’ cultivars characterized by different biological and agronomical traits to which shadings were imposed in July and August. Histological analysis was carried out from summer onwards in order to determine the evolution of floral bud differentiation, and the acropetal progression of primary xylem differentiation along the flower bud axis. Periodical recordings to evaluate the bud drop, blooming time, flowering and fruit set rates were performed also. These shade treatments determined a temporary shutdown of floral differentiation, slowed xylem progression up to the resumption of flower bud growth and a reduced entity of flowering and fruit set. These events were particularly marked in ‘San Castrese’ cultivar, which is well known for its adaptability to different climatic conditions. These findings suggest that adequate light penetration within the canopy during the summer season could be the determining factor when defining the qualitative traits of flower buds and their regular growth, and ultimately to obtain good and constant crops. Keywords: Floral differentiation • Xylem vessels • Bud growth • Bud drop • Fruit set © Versita Sp. z o.o.

1. Introduction In apricot, as well as in other deciduous fruit species, floral bud initiation, differentiation and organogenesis take place during the summer season that precedes anthesis and are achieved by a variety of environmental as well as intrinsic cues [1]. The flower-bearing bud development is a process requiring the transformation of an undifferentiated meristematic apex into a structure carrying flowers throughout three main steps: induction, with production of a ‘floral stimulus’ in the leaves; translocation of the ‘floral stimulus’ towards the meristems; evocation throughout the involvement of molecular genetic mechanisms [2], followed by the floral morphogenesis. During these processes, a sequence of morphological and biochemical changes

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occur such as cell division, increased carbohydrate content and activity of some respiratory enzymes, protein and RNA synthesis [3,4]. Environmental factors (temperature, solar radiation, water availability), abiotic stresses occurring before and during the differentiation phase as well as certain cultural practices (i.e., time and type of pruning, training system, fertilization, irrigation, chemical treatments) have been identified as important triggers that are able to modify the regularity of the floral differentiation phase [5-7]. In particular, it has been observed that different light levels available within the canopy throughout the growing season, and a lower interception of photosynthetically active radiation (PAR) such as that occurring at the base of the ‘Y’ training system, negatively affect the earliest floral morphogenesis phases [8]. These authors found * E-mail: [email protected]

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that, similarly to other species, in the shaded zone of the canopy there were fewer fruiting shoots with fewer differentiated flower buds. These disorders, compromising the bud and flower quality of the next season, may cause a lack of fruit set, as a consequence of a flower bud drop which in apricot has been repeatedly observed in different cultivars and environmental conditions [9-11]. A regular progress of the first phases of flower bud differentiation should be assured also by the development of the vascular traces consisting of elongated procambial cells that provide a ring of vascular bundles [12]. In concomitance with the development of floral whorls, the transition from procambial tissues to xylem cells occurs producing the vascular elements, i.e. dead cells with lignified walls producing an empty conduit [13]. Xylem vessels develop from the base of the bud axis up to the floral primordium, reaching the rudimentary sepals and petals, then the anther filaments, and finally the pistil [14]. An irregular xylem differentiation, and the lack of xylem connection between the flower bud axis and the floral primordium prevent the acropetal transport of fundamental elements (i.e. potassium, boron, carbohydrates), which plays a significant role in determining ‘bud quality’ [15,16]. Thus, a regular development of flower buds assures constant crop productivity that may be strongly reduced in environments with high summer temperature, high radiation, and high water vapor pressure deficits [17,18]. To avoid these situations in horticultural crops, shading nets have been used to reduce the radiation load also in several fruit species such as citrus and sweet cherry [19,20]. This practice has been proposed for apricot cultivation too in scarcely irrigated and highly insolated areas typical of Mediterranean climates [21]. The use of shading, to reduce the net radiation in the canopy, would determine a proportional decrease in transpiration, avoiding a water deficit [22]. Considering that key processes related to the flower biology start during the

summer season, the knowledge of how shading can affect them is essential to obtain the best biological responses from the cultivated trees. The aim of this investigation was to assess whether imposed summer shading treatments in apricot (Prunus armeniaca L.) can affect the main phenological phases related to the floral morphogenesis (floral differentiation, xylogenesis), flower bud growth and quality in terms of bud capacity to set fruit. For this purpose, two apricot cultivars characterized by different biological and agronomical traits were analyzed.

2. Experimental Procedures 2.1 Plant material and growing site

The experimental trials were carried out on ‘San Castrese’ and ‘Stark Early Orange’ (SEO) apricot cultivars (Table 1), over a whole annual cycle (2008-2009). Cultivars were grown at the research station of the Department of Tree Science, Entomology and Plant Pathology (University of Pisa) located in the Tuscan coastal area (Venturina-Livorno-Italy, altitude 6 m, lat. 43.02°N, long. 10.36°E). Trees were arranged in a block design, grafted onto ‘Myrobolan 29/C’ rootstock, and trained to free palmette system (5x4 m) with a row facing East-West. All trees received routine conventional horticultural care.

2.2 Shading experimental design

The study was a completely randomized design and each treatment consisted of four replicate trees. Fully-grown apricots were covered in postharvest by suspending neutral shading nets of green polypropylene, 1 m above the trees by a rigid structure. Two shadings were imposed during the summer season (Table 2): the first in July (S1), the second in August (S2). Shading nets were removed one month after the beginning of each treatment. The

Cultivar

Parents - Origin

Chilling Requirement (CR)

Tree and fruit characteristics

San Catrese

- Unknown - Italy, Vesuvian area (Naple)

Medium (about 900 CU) Viti et. al. [38]

Standard growth habit; 2-3 flower buds/node (fertility index) High environmental adaptability; High and constant crop Susceptible against PPV virus Early blooming time Medium fruits, fair flavour, dual purpose stone fruit

SEO

- Unknown - Grandview Washington, USA

Very high (>1400 CU) Viti et. al. [38]

Upright growth habit ; >5 flower buds/node (fertility index) Scantly environmental adaptation ; inconsistent crop Resistant against PPV virus Late blooming time Big fruits, appreciated for flavour and colour

Table 1.

Main biological and agronomical traits of ‘San Castrese’ and ‘Stark Early Orange’ (SEO) cultivars.

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The effect of summer shading on flower bud morphogenesis in apricot (Prunus armeniaca L.)

Thesis

Dates Start

End

Days from starting trial

Shading 1

July 5

August 5

S1+30

Shading 2

August 5

Control

Table 2.

September 5 Full sun exposure

S2+30 C; C+30; C+60; C+150

Shade treatments (S1 and S2) with starting and finishing dates of experiments carried out on ‘San Castrese’ and ‘Stark Early Orange’ cultivars.

Figure 1.

Developmental stages of meristematic apices. Stage A (x400; scale bar: 50 μm): undifferentiated meristematic apex rounded shape, during the ‘induction’ phase (‘tunica’: external zone of the meristematic apex constituted by three layers of cells; ‘corpus’: under the tunica constituted by mother cells). Stage B (x400; scale bar 50 μm): differentiated meristematic apex with receptacle primordium arrangement, raised shape, after floral ‘evocation’ phase. Stage C (x 200; scale bar: 200 μm): sepal primordial. Stage D (x100; scale bar: 200 μm): petal primordial. Stage E (x100; scale bar: 200 μm) stamen and pistil primordial. (r: receptacle; s: sepal; p: petal; st: stamen; pi: first appearance of pistil).

control (C) was represented by trees maintained under natural conditions with full sun exposure. Photosynthetically active radiation (PAR) was measured using a Ciras 1 Portable Photosynthesis System (HitChin, Hertford shire, UK): the shade net intercepted 90% of the incident radiation. At midday on a sunny July-August day, the light intensity was 160 µEm−2 s−1 under the shade cloth and 1650 µEm−2 s−1 outside.

2.3 Histological analysis

Sampling started just before the first shade treatment of July and was periodically carried out until early spring on both shaded and trees exposed to full sunlight (control) in order to determine: a) the evolution of floral differentiation and b) the acropetal progression of primary xylem differentiation along the flower bud axis. a) To establish the floral differentiation stage, the meristematic apices (25 per each sampling time and cultivar) were periodically collected, from the median portion of one-year-old fruiting shoots, cut from the west orientation and top position of the canopy [23]. The apex collection covered a period of 120 days, from July to the beginning of leaf drop. The meristematic apices were fixed in a FAA solution (55% ethanol, glacial acetic acid, 10% formaldehyde; 8:1:1 v/v). b) To follow the acropetal progression of primary xylem differentiation along the flower bud axis, flower buds (n=25 per each sampling time and cultivar) were 56

Acronym

collected from the same position of shoots as described above. From summer to the end of winter, flower buds were excised with a small portion of twig and fixed in Farmer (ethanol and glacial acetic acid 3:1 v/v) and subsequently prepared for the anatomical observations. Both apices and flower bud samples, once rinsed in water, were dehydrated in a graded ethanol series, embedded in histoplast and then longitudinally sectioned (10 μm), using a Shandon microtome. The slices were then de-waxed, re-hydrated in an ethanolwater graded series. Meristematic apices were stained with 1% acqueous safranine O and fast green (0.2%) and mounted in Synthetic Mountant (Shandon). The slides were observed under an optical microscope (Nikon, Fluophot) whit polarised white light. The floral differentiation stage (Figure 1) was assessed according to Andreini and Bartolini [24]: stage A = undifferentiated meristematic apex constituted by ‘tunica’ (external zone of the meristematic apex constituted by three layers of cells) and ‘corpus’ (under the tunica constituted by mother cells); -stage B = receptacle primordium arrangement; -stage C = sepal primordia; -stage D = petal primordia; -stage E = stamen primordial and first appearance of pistil. Flower bud sections were stained with acridine orange (stock acridine orange 0.1% in 1⁄9 Walpole’s buffer pH 4.2). Slices were examined using a Nikon epifluorescent microscope equipped with a 100 W mercury lamp plus an excitation filter (B, type IF 420–490 nm).

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The acropetal progression of primary xylem differentiation along the flower bud axis was defined by the following stages (Figure 2): stage 1 = at the base of the axis; stage 2 = at ½ of the axis; stage 3 = at ¾ of the axis; stage 4 = at the base of the ovary; stage 5 = inside the pistil [14]. Representative selected sections from both procedures were photographed with a digital camera (Olympus C-2000 z) equipped to the microscope.

2.4 Measurements under field conditions

One-year old fruiting shoots (10 per tree) were labelled in each treatment to evaluate the influence of shading on the current and next season’s flower bud growth. The following parameters were recorded: a) initial flower and vegetative bud number; b) monthly count of the persisting flower buds for the evaluation of bud drop; c) blooming time expressed as Julian Day (JD 1= January 1st); rate of bloom, determined as F50 when 50% of flowers were open, and d) fruit set. Over the year, meteorological data (rainfall, minimum and maximum daily temperatures) were recorded. Starting from 50% of leaf drop, hourly temperatures were registered by an automatic data-loggers (Tynitag Plus®, West Sussex, UK, 2003) and transformed into Chill Units (C.U.) to quantify the amount of chill received by the plant [25].

2.5 Statistical analysis

Statistical analysis was performed using the Statgraphics Plus software, version 5 (Manugistics, Inc., USA). Prior to analyses, data were log, square-root and squaretransformed to satisfy normality and homoscedasticity assumptions. Differences concerning flower bud drop, flowering and fruit set percentage between treatments were tested by Student’s t- test procedure. A probability level of P≤0.05 was considered to be statistically significant.

3. Results and Discussion 3.1 Influence of shading on floral differentiation

The histological analysis of meristematic apices, carried out during the summer-autumn season, permitted distinguish the different stages of floral differentiation. ‘San Castrese’ and ‘SEO’ cultivars showed differences in flower bud initiation also in trees exposed to full sunlight. In ‘San Castrese’ (Figure 3A), just one day before the first shade treatment (C), in 20% of apices the receptacle appeared (stage B); another 20% of buds were vegetatively differentiated and the remaining apices

Figure 2.

Representation of xylem vessel differentiation along the flower bud axis, taken from Bartolini et al. [14]: stage 1 (at the base of the axis); stage 2 (at ½ of the axis); stage 3 (at ¾ of the axis); stage 4 (at the base of the ovary); stage 5 (inside the pistil). Dotted line indicates the pulvinar juncture.

(60%) showed morphological features of undifferentiated buds (stage A). After one month, in control trees (C+30), a marked appearance of meristematic apices at stage D (petal primordia) was observed. On the other hand, in shaded trees (S1+30) the percentage of apices at stage B was similar to that recorded just before the start of treatment (C), and only an increase in vegetative buds was observed. After one month passed from the second treatment (S2+30), shaded trees showed an increase in vegetative apices and the rate of those differentiated at stage D were 40% as recorded in control trees (C+30), at the time of shading. In full sun trees (C+60), a more advanced stage was observed: 60% of apices were at stage E (stamen primordia) and a very low percentage was undifferentiated. At the beginning of dormancy phase (November), differences between shaded (S1+120; S2+90) and full sun trees (C+150) were not found: 65% of examined apices were completely differentiated (stage E) and the other 35% were vegetatives. In ‘SEO’ cultivar (Figure 3B), the floral differentiation took place later than San Castrese so that, before the first shade treatment (C), 80% of apices examined were at undifferentiated stage. This same state was observed at the end of the first shading (S1+30) while, at the same time, samples collected from full sun trees (C+30) showed 50% of differentiated apices at stage B. The second shade treatment (S2+30) also altered the 57


differentiation process: the percentage of apices always at stage B was the same recorded just before the beginning of treatment (C+30). In control trees (C+60), a progress in floral differentiation was observed (stage C, corresponding to the appearance of sepal primordial). In November, no differences were noted between shaded or trees in full sunlight and apices at stage E were more than 60%, as observed in ‘San Castrese’. The comparison between the two cultivars, under control conditions, showed a delay of floral differentiation in ‘SEO’. In this cultivar, the morphological changes of meristematic apices denoting the beginning of floral differentiation (stage B) took place in August, about one month later than ‘San Castrese’. Both shade treatments affected the floral differentiation of cultivars, leading to a temporary shutdown of the process regardless of the stage reached at the pre-treatment time. After removing the shading nets, meristematic apices were able to recover their development, though slower development was observed. The delay of flower bud differentiation affected

Figure 3.

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by shading conditions could be attributed to a decrease in daily amounts of phloem sap received by the apices. Recently, Morandi et al. [26] in consequence of an early season shading on apple trees observed a reduction of assimilates fixed by the canopy photosynthesis. The low PAR available was responsible for the lowest carbohydrate levels at the time when crucial events of apricot floral morphogenesis took place [8], caused by altered nutritional or hormonal status [20].

3.2 Influence of shading on xylem differentiation

The anatomical observations carried out on flower buds showed a progressive differentiation of the secondary thickness of procambial cells in the xylem vessels. The growth-rate varied with genotypes and shade treatments producing a different temporal pattern (Figure 4). ‘San Castrese’ showed regular xylem differentiation from summer onwards (Figure 4A), and the sequence of different xylem stages was identified from stage 1 (xylem vessels at the base of the flower bud axis) to stage 4 (xylem vessels up to the ovary). Both shade

Distribution (%) of flower (FB), vegetative (VB) and undifferentiated (UB) apices recorded from July to November in ‘San Castrese’ (A) and ‘Stark Early Orange’ (B) apricot cultivars: - in control trees (C; C+30; C+60; C+150 days from starting trial); - in shaded trees after 30 days from treatments (S1+30; S2+30); - at the beginning of dormancy phase in November. Capital letters within white bars showed the most advanced stage of floral differentiation.

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Figure 4.

Distribution (%) of xylem vessel differentiation stages (from stage 1 up stage 4) detected in flower bud axis during the summer (JulySeptember), autumn (October-November) and winter (December-February) seasons in shaded (S1, S2) and full sun trees (C) in ‘San Castrese’ (A) and ‘Stark Early Orange’ (B) apricot cultivars.

treatments (S1, S2) gave slower xylem progression than controls, right from the start of the summer season. This trend was also noted in the Autumn-Winter samples from shaded trees in August (S2) where flower buds were still at stage 1. On the other hand, at the end of winter, all the examined buds from full sun trees were at stages 3 and 4, corresponding to an advanced xylem differentiation up to ¾ of the bud axis and at the base of the ovary, respectively (Figure 5A). In ‘SEO’ cultivar, flower buds showed an irregular progress of xylem differentiation and the most advanced stage (stage 4) was not found, also in the control trees (Figure 4B). During the summer season, stage 1 was the only one recurrent in both shaded and no shaded trees. In autumn, the appearance of stages 2 and 3 was only observed in samples from full sun trees, although

in a small percentage. More marked differences were observed at the end of winter: while in flower buds of both shading treatments stage 1 was prevalent (Figure 5B), about 80% of control flower buds showed xylem vessels up to ½-¾ of bud axis (stage 2 and 3).The differences in xylem process evolution, observed in both cultivars, confirm previous results reporting a regular cell differentiation of vascular elements for ‘San Castrese’ and an irregular xylem growth for ‘SEO’ [27,28]. In both cultivars, shade treatments determined a slow xylem differentiation up to the resumption of flower bud growth (end of winter). In particular, the second shading in early August had a more prolonged negative effect noticeable by the achievement of a less developed xylem stage, in comparison to non-shaded trees. The compensatory capacity for the flower bud 59


Figure 5.

Representative longitudinal sections of flower buds collected at the end of winter showing a different xylem development: stage 3-4 in ‘San Castrese’ (A); stage 1 in ‘SEO’ (B). Arrows show the xylem vessels stained by acridine orange reaction under epifluorescent microscope (x 40; scale bars: 150 μm).

differentiation progress found in meristematic apices, when light intensity was restored during summer, was not verified. Our results suggested xylogenesis is a process particularly sensitive to a decreased light intensity, which might interact with inductive signal such as metabolic substances and phytohormones that play a regulatory role in the control of primary vascular differentiation [29,30]. Different levels of auxin, together with other signaling molecules, such as cytokinin and growth factors, might act as a patterning agent for differentiation of vascular tissue [31,32].

3.3 Influence of shading on flower bud development During the autumn-winter season of 2008-2009 temperatures were favourable for a good chilling accumulation (Figure 6): 1000 CU were recorded early, at the end of January and a high CU amount (more than 1500 CU) was recorded on March 1st. These conditions were able to satisfy the chilling requirement of both cultivars allowing a regular dormancy release of flower buds. Late frost episodes did not occur and a good amount of rainfall was detected from summer to spring (about 350 mm). In both cultivars grown under full sunlight, the evolution of flower bud growth was similar to those observed in several previous years [33,34]. ‘San Castrese’ (Figure 7) confirmed its ability to reach regularly the blooming time occurred at the first decade of March (65 JD) with a satisfactory entity of flowering 60

(45%) and fruit set (10%). ‘SEO’ cultivar flowered late, 17 days after ‘San Castrese’ at the end of March (83 JD), and had a high percentage of flower bud drop (about 90%) with a scanty flowering percentage (10%), and rather low fruit set (Figure 7), confirming the complexity of its flower biology. The poor results of ‘SEO’ cultivar were not altered by the shading treatments. On the contrary, shading led to a reduction in the entity of flowering of about 30% with respect to the control trees in ‘San Castrese’, although they were not reflected in the blooming time, as found by Lugassi-Ben-Hamo et al. [35] in other species. A very low fruit set was recorded as a consequence of an increased bud drop. This effect could be due to the delay of xylem differentiation linked to a high appearance of bud necrosis (data not shown). An irregular xylem differentiation, not assuring the acropetal transport of fundamental elements (i.e. potassium, boron, and carbohydrates), can play a significant role in determining the ‘bud quality’ [15,16,36].

4. Conclusions This study shows that shadings during the summer season in apricot can lead to delayed effects in the year after treatments, as found in other species [37]. Shadings negatively influenced the evolution of flower bud development, as indicated by irregular floral morphogenesis and xylogenesis.

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Figure 6.

Minimum and maximum daily temperatures and rainfall (bars) recorded during the experimental period, from July (2008) to April (2009). The Chill Units (C.U.) accumulated during the autumn-winter period are shown.

Figure 7.

‘San Castrese’ and ‘Stark Early Orange’ (SEO) apricot cultivars. Percentage of flower bud drop, flowering and fruit set recorded in shaded (■) and full sun trees (□). The asterisk (*) denotes significant differences between shaded and control trees within each stage by Student’s t test (P≤0.05).

The irregular growth of flower buds from shade trees was proved by a greater bud drop that occurred just before the blooming time with a consequently sensible reduction of flowering and fruit set rates. These events were particularly marked in ‘San Castrese’, which is well known for its adaptability to different climatic conditions. On the other hand, ‘SEO’ was apparently less influenced by the shade treatments which did not alter the poor bud quality of this genotype that generally shows serious problems in floral morphogenesis by early appearances of anomalies determining a dramatic increase of flower buds not able to flowering and fruit-set [9,27,38]. Focusing on the performance of ‘San Castrese’ cultivar, these findings suggest that shading, producing

an inadequate light penetration within the canopy during the summer season, could reduce the flowering rate in the year after treatment. The low PAR available could be responsible for the different nutritional status of flower buds on the shaded part of the canopy which showed the lowest carbohydrates levels at the time when crucial events of floral morphogenesis take place [8,35]. Hence, the use of shading nets in apricot culture in areas characterized by scarce irrigation water and high insolation could be a detrimental practice to be taken with great care. Moreover, the choice of managements that allow adequate light penetration within the canopy could be determining factor when defining the qualitative traits of flower buds in order to obtain good and constant crops. 61


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