THE ECOPHYSIOLOGY OF CARBON IN FRUIT TREES: A DRIVER OF PRODUCTIVITY, A TOOL TO FACE CLIMATE CHANGE, A PRODUCER OF INNOVATION THAT CAN BECOME TOMORROW'S GROWING PARADIGM Luca CORELLI GRAPPADELLI, Brunella MORANDI

Dipartimento di Colture Arboree, University of Bologna, V.le Fanin 46, 40127 Bologna, Italy Corresponding author e-mail: luca.corelli@unibo.it Abstract The control of tree performance by exploiting the interactions of tree and environment is among the goals of ecophysiology. This discipline has accompanied genetic improvement of tree crops over the last half century, and has provided the scientific bases of orchard efficiency and productivity. High density plantings have their roots in the knowledge of the interactions between trees and incoming radiation. Pruning, thinning, water management and other cultural practices are based on similar knowledge. The continuing efforts in elucidating the relationships between environment and trees/tree parts are now focusing on organs such as the fruit, which is becoming an integrator of the plant’s well being: if fruit grow as expected (when measured precisely) they reveal/confirm a healthy status and proper management of the tree. Current knowledge on tree water relations, fruit development, and their determinants at the vascular level are paving the way for future innovation in the management of irrigation, that will allow to better tailor water restitution to the tree needs on a daily, instead of a seasonal, scale. Similarly, knowledge of the complex relationships between incoming light and tree performance promises to allow to maintain orchard productivity and quality while consuming less water. The role ecophysiology can play to offset climate change stems, along with the benefits deriving by a smarter use of renewable resources leading to a smaller water print and energy uptake, also from the capacity that orchards have to sequester Carbon. There is a growing body of knowledge that is amenable to innovation transfer and technological uptake, which will likely form the backbone of precision fruit growing, which will in turn allow to gauge and control in real time the development of the crop, giving the grower the possibility to change his/her management according to the actual orchard needs. Key words: fruit growth, light conditioning, precision fruit growing, source-sink relationships, water management INTRODUCTION The physiology of Carbon in fruit trees is of paramount importance in fruit production: from an evolutionary point of view, fruit trees aim to produce and disperse the highest amount of seed, the fruit being a very sophisticated vehicle for such dispersal. As it happens, fruit growers are not interested in high production of seeds, but of what makes them so attractive to potential agents of dispersal: the fruit. Over the ages, man has learned many ways (encompassing breeding and management techniques) to govern tree growth towards this goal. The modern orchardists employ the latest available knowledge to improve on existing solutions. This continuing effort has its roots in the need to maintain economic viability and, more recently, in the pressing demands that environment, renewable resources and energy

inputs be considered as important factors in fruit production as productivity and quality themselves. Ecophysiology deals with the interaction of plants and the environment. At a time when climate change is a threat, ecophysiology is ideally placed at the frontier of current research aiming to maintain orchard profitability in a new environmental set of conditions. If ecophysiology is to remain as important as genetics in determining orchard performance, it will have to continuously release information to the growers who will then be able to improve their operations by adoption of newly available knowledge. The exciting news from ecophysiology is that it is well equipped to meet this challenge. Following is a brief survey of the “classic” knowledge and a vision on how its developments will be able to continue supporting growers in their endeavour.

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AgroLife Scientific Journal - Volume 1, 2012CD-ROM ISSN 2285-5726; ISSN-L 2285-5718

The impact of ecophysiology on fruit quality and orchard productivity Light interception and orchard productivity The basis of orchard productivity lies in the interaction between the tree and sunlight. Not only must light be intercepted, but also well distributed within the canopy. Therefore, the grower must achieve a high light interception in the shortest possible time (main advantage of high density systems), while maintaining by proper pruning an open canopy, where no shading occurs, which may not be so easy in the presence of very closely spaced trees, particularly if under vigorous conditions. The early work of Heinecke [11], Jackson [13] and Cain [3] in fact demonstrated the need to couple light interception with distribution within the canopy: they agreed that at least 30% of the incident light was needed to ensure fruit color, quality, and to ensure flower bud differentiation. The amount of light intercepted by a plant is linearly related to the amount of dry matter it produces [23]. This does not automatically translate into high yields as partitioning of the photosynthetic products into marketable apples must not be taken for granted: mechanisms of competition for resources are always at work during the season, and the fruit is a weak competitor in the early part of its growth cycle. Researchers have shown that in properly managed, efficient orchards, yield of marketable apples increases linearly with the percentage of light intercepted. The relationship, however, is not clear cut: from his collation of published data, Lakso [15] showed that at values greater than 50% light intercepted, both very high or very low yields have been reported (Fig. 1). Many modern training systems strive to achieve this balance of high light interception and good distribution, making full use of dwarfing rootstocks and other vigor-controlling techniques. The slender spindle training system allows to optimize light interception/distribution for low vigor environments, such as are common in northern Europe, or in Alpine environments, but many modern training systems have been designed to improve this aspect as reviewed by Robinson [34]. It is interesting that without failure the same physiological principles are applied

everywhere, although they lead to different solutions, because of the different environments

Fig. 1. A compilation of third party data depicting the relation of orchard yields to Photosynthetically Active

Radiation intercepted by the canopy, for different training systems and planting densities. For full

explanation see [15] where the systems have been developed. Adapting the solution to local environments is one of the key factors to successful implementation of the physiological knowledge available. If one considers the characteristics of virtually all the training systems that have been developed, it is easy to find a close relationship between the training system and the environment where it was developed. For example, the HYTECH system [1] was designed to reduce fruit sunburn damage by using vegetation as a natural screen for sunlight, a considerable problem in the apple-producing region of Washington State. From the above discussion, it can be concluded that not in all environments maximum light interception is necessarily the best goal. Under conditions of high light intensity and low precipitation (unless sufficient water is available), one may question whether training systems that expose the leaves to very high light levels for a very long time during the day are so desirable. Source-sink relationships Leaf Demography. Source leaves are needed to generate carbon flows towards vegetative and reproductive sinks. Different leaves may have a different role and impact on tree productivity because of several factors: the light environment where the buds have differentiated, the current season light

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environment under which they have developed (determining their light/shade characteristics), the type of leaf (spur vs. shoots). A linear relationship was found between spur leaf area and yield per tree in apple (Fig. 2), but not for either shoot leaves or for total tree leaf area, the main reason being that spur leaves support fruit growth early in the season, before and at the time of fruit set [38, 6]. A similar role for the leaves of the shoot emerging from the axil of a node carrying a fruit has been indicated for peaches as well [7]. These findings illustrate the need for an efficient, well developed leaf area early in the season, when fruit growth is by cell division, and the potential for fruit size is set.

Fig. 2. Relationship between cumulative spur-leaf area and cumulative yield per tree, according to training system, for

mature apple trees (Golden Delicious/M9) The importance of partitioning. In fruit trees, resources are allocated to different growing sinks, of which only fruit has a commercial value. Fruit grow by accumulation of water, photoassimilates and other phloem and xylem sap components. Carbohydrates are translocated from source leaves via a process beginning with their loading into the phloem, transport and unloading into sink organs. The process determining how much carbon is translocated to the different types of sink (vegetative vs. reproductive) is normally termed “assimilate partitioning” and can be limited both by the amount of carbon available for export (source limitation) and/or by the capacity of the different organs to import carbon (sink limitation) [39, 8]. A source limitation may depend on photosynthetic activity, sugar synthesis in the leaf, or on phloem loading, while sink limitation is a

function of the sink ability to attract assimilates (sink strength). Without continuous supply of carbohydrates, fruit cannot grow. Assimilate partitioning is a complex phenomenon which can be controlled through many cultural techniques, among which pruning, fertilization, crop load management and irrigation are the most effective. For example, flat, well illuminated canopies (palmette and minibush/minispindle) produced about 50% more apples/leaf area units than did bushy-type trees [36], which had less uniform light distribution profiles [5]. The effect of crop load on fruit growth. Crop load strongly affects resource availability, as source organs may not be able to supply sufficient resources to all growing sinks [32, 8]. Furthermore, crop load negatively affects leaf, stem, and fruit water potentials [21, 29], thus changing the hydrostatic pressure gradients along the vascular paths. This may affect vascular flows delivering water and carbon to the fruit, as resource translocation responds to hydrostatic pressure gradients in the phloem and xylem vessels [28]. Thus, perhaps unexpectedly, the impact of crop load on fruit growth is twofold, as on one side it reduces the amount of carbohydrates available to each fruit and on the other it makes it more difficult for the fruit to attract water and solutes. As a result high crop levels reduce fruit growth rates and size at harvest. On the other hand, a moderate to high crop level may limit vegetative growth, and improve light distribution into the canopy. Furthermore, a high assimilate demand from reproductive sinks has been found to enhance the photosynthetic performance of leaves [10]. Managing fruit size and yield: thinning and monitoring fruit growth. The relationships between crop load, fruit size and yield are not linear (Fig. 3). At high crop loads reducing fruit number brings about a more than proportional increase in fruit size. At low crop loads however, size no longer responds to fruit removal. A similar (but opposite) relation holds between crop load and yield: a more than

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Fig. 3. Responses of mean fruit weight (a) and total tree productivity (b) to crop load (expressed as fruit number per cm2 of trunk sectional area- TCSA) for ‘Red Gold’

peach trees, during two consecutive seasons. The arrows indicate the crop level (corresponding to 1.5 fruit cm-2

TCSA) at which the best compromise between quantity (yield) and quality (fruit weight) is obtained for the cultivar considered in the Po Valley environmental

conditions proportional initial response of yield to crop load is followed by a diminishing response in which the decreasing fruit size offsets the increase in fruit density, so that even though yield may still increase its economic value does not. Fruit quality in fact is more readily affected than yield at commercial crop loads. The challenge to the grower then becomes that of setting crop loads to the most profitable levels which, under current market conditions, means striking the “yield/fruit weight” balance which returns the maximum economic revenues. This balance is achieved, for those crops which set excessive fruit numbers, via thinning, which aims to minimise fruit-to-fruit competition since the earliest phases of fruit development. However, reliable indicators that the appropriate crop load has been set are still lacking and it will be a task for future research to achieve this result. Seasonal fruit growth. Fruit size at harvest can be defined as the product of fruit cell number, times cell volume, plus intercellular space. The early stages of fruit development are characterized by an intense cell division which is subsequently followed by cell expansion [33]. In temperate fruit species, endogenous (e.g. crop load and leaf type) and environmental

factors (mainly temperature) are known to affect the cell division process, thus impacting on the potential of fruit development that is achieved [40, 37]. The dynamics (e.g. time, rates) of fruit cell division and cell expansion result in a seasonal growing pattern which may be different depending on the species. These patterns may be described in terms of diameter, volume or weight by use of different models, which represent useful tools to monitor the fruit growth performances during the season. Water relations The functions of water within plants are numerous, of which the most important is to provide a means for leaves to control their temperature via the liquid-to-gas phase change which consumes some of their heat load and which generates the transpiration stream towards the atmosphere. This of course requires stomata to be open. In turn, open stomata allow CO2 influxes that sustain photosynthesis. In addition to these functions, movement of mineral and organic resources within a tree is permitted/regulated by the plant capacity to generate potential gradients within its different parts. Growing sinks (which include fruit and growing shoot tips) rely on the existence of these gradients to attract the resources they need for their growth and survival. Regulation of the balance between vegetative and reproductive growth can be achieved via proper management of water supply through irrigation, as in the “classic” regulated deficit irrigation (RDI) approach proposed over three decades ago [22]. Management of tree water relations via irrigation has thus become one of the most important tools to control tree productivity and fruit quality worldwide. Instrumentation and scientific knowledge have been developed to detect stress-conditions both in the soil and in the tree. Based on this knowledge, irrigation strategies have been developed, for example to allow limited stresses in certain parts of the season (the RDI approach) and to ensure their avoidance during other phenological stages. Surprisingly, to date no one has been using the fruit as a more direct indicator that irrigation is properly applied. This is a shift of paradygm that will be made in the near future.

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Climate change and fruit growing Under changing climates, several phenomena are expected to occur, at global and regional scales, which have the potential to impact fruit production, including increased heat- water-stress conditions [12], changes in crop phenology, but also geographical shifts of the growing areas of several fruit species. Long term comparisons of meteorological data indicate earlier occurrence of blooming, harvest and leaf drop in apple of up to 10 days for central Europe [14]. Further, the expansion of grapevine and olive cultivation towards Northern and Eastern parts of Europe has been reported over the last 20 years [30]. It is expected that higher ambient temperature will lead to increased plant organ respiration and reduced plant water use efficiency, with detrimental consequences on biomass production (yield) and product quality [30]. Higher evapotranspiration and reduced precipitation will result in a strongly negative climatic water balance [35] which has to be compensated through irrigation systems to ensure sustainable production. These changes are expected to impact more the European Mediterranean countries which are the most exposed to temperature rises and water scarcity while irrigation needs in this area are expected to increase up to 20-30% by 2020 [9]. Horticulture and fruit growing in particular risks much by climate change, but has also much to offer. Recent ecophysiological studies on improvement of orchard sustainability via innovative management of light and water relations are showing the possibility to maintain (and even increase) current quality and production levels with much decreased use of these renewable resources. On the other hand, fruit growing can also act as climate change mitigator since orchards are capable of storing up to almost 3 tons of carbon per hectare per year, according to the most accurate and recent estimates for apple (Tagliavini et al., personal communication). From Ecophysiology to Innovation In a world scenario increasingly demanding improved sustainability of fruit growing, ecophysiology has much to offer. In fact, knowledge generated in basic studies is becoming more and more available that can

influence the way the growers of tomorrow will manage their orchards. A very brief survey of some of the more promising examples might include the following. Maximising light interception is not always the best choice Solar radiation and dry matter production are bound by a curvilinear relation. At single leaf and sometimes at whole canopy level [18], net photosynthetic rates increase linearly with irradiance until a saturating point is reached. As light limitation has a negative effect on carbon assimilation, excessive light levels can also be negative and, rather than improving it, they can increase the photo-oxidation phenomena which result in reduced carbon assimilation [4]. Both the photosynthetic apparatus and chloroplast structures are the targets of oxidative molecules, which can cause photodamage. The direct consequence is the reduction of leaf photosynthetic performance. As the consequences of photodamage can be dangerous for them, plants have developed an effective and efficient recovery system, and several reactive/adaptive answers are activated to sequester/inactivate the reactive oxygen species (ROS) produced, or to limit their oxidative power. The recovery process, necessary for plant survival, requires the consumption of resources (water/assimilates) [4], derived from the plant dry matter pool and thus potentially subtracted from the main sinks: fruit. From early studies it has been estimated that during a summer day about 7-8% of total carbon assimilated is needed to repair the damaged photosystems. Current technologies already allow recovery of this loss, as hail net trellising could also be used to support light shading materials to reduce the amount of excessive energy reaching the canopy. An added benefit would be the drastic reductions in water consumption. Recent studies have shown how the use of 40% neutral shading nets may reduce the water use of a peach orchard as much as 30% without any loss in dry matter accumulation [19] (Photo 1).

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Photo 1. Peach orchards subjected to different light and micro-environmental conditioning: reflective mulching,

control and shading Heavy neutral shading in the early stages of fruit growth causes fruit abscission to an extent comparable to chemical- or hand-thinning [2, 42]. Hail net trellising could also be used to support these shade nets, thus making the trellis more cost-efficient. Studies carried out in Switzerland have demonstrated that this approach is already economic viable in organic apple production where inexpensive chemical thinning is not allowed (Bravin et al., personal communication). This is but one of the potential advantages that the exploitation of the light environment in the orchard could permit. Commercially available coloured hail nets may in fact allow to control tree morphogenesis. The effects include bud breaking, shoot elongation, leaf photosynthesis, water use efficiency and also fruit growth. The challenge is to optimize the light transmission spectra (via adoption of novel high-tech materials) so that as many of these responses as possible can be obtained. Fruit growth however is more complex than it appears and needs to be evaluated primarily under a source-sink relationships point of view. Moving from seasonal to daily fruit growth scale The availability of accurate and precise devices to monitor fruit growth [26] has allowed to move from a seasonal to a daily scale in the study of fruit growth (Photo 2). Indeed, recent studies in several fruit species, including peach [27], kiwifruit [24] and apple [17] have shown how fruit diameter alternates periods of swelling and shrinkage during the 24 hours.

Photo 2. Custom-built fruit gauge developed at the

University of Bologna, used for the accurate monitoring of fruit diameter variations

The precise monitoring of fruit diameter variations during the day has also allowed to determine the daily patterns in the phloem, xylem and transpiration flows to/from the fruit [17] (Fig. 4). These studies provide information on the amounts of water and carbohydrates flowing to the fruit at different times during the day and how they respond to changes in the fruit environmental conditions [27]. Anatomical and biochemical differences led fruit belonging to different species to adopt different growing strategies in terms of diurnal vascular flows and phloem unloading. Undergoing research in this field is showing that transport of carbohydrates from the phloem to the fruit tissue (phloem unloading) occurs through passive (via biophysical gradients) or active (via specific sugar transporters) mechanisms [16, 31].

Fig. 4. Diurnal courses of fruit relative growth rate,

specific phloem, xylem, transpiration flow rates (mg g-1 min-1) and VPD (kPa) for ‘Red Gold’ peach fruit during the cell expansion stage. Data were recorded at 6 minute

intervals and each line is the mean of 5 fruit

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These strategies may also change during the season, as fruit anatomy can undergo modifications with fruit development. For example, during the season, peaches exchange increasing amounts of water from the fruit to the atmosphere. The growth of this fruit is based on high water imports via xylem flows, while carbohydrate transport is facilitated by water losses via epidermal transpiration, which decreases the fruit pressure potential and increases the hydrostatic pressure gradient necessary for passive phloem unloading to occur [25]. On the other hand, the apple fruit transpires decreasing amounts of water during the season due to the decreasing permeability of its cuticle. In these conditions, the hydrostatic pressure gradients between phloem and fruit tissue, that are necessary for passive carbohydrate transport to occur, cannot be maintained. For these reasons, in apple, specific carbohydrate transporters are present in the fruit apoplast to actively unload the sugars from the phloem to the fruit cells [41]. This information will lead growers to modify their cultural practices for different species, in recognition of the marked differences in their growth physiology. In peach, for example, the high fruit transpiration rates play a pivotal role in water and dry matter import into the fruit [25], and enhancing VPD (i.e. via reflecting mulches) (Photo 2) may positively affect fruit growth and quality. New irrigation strategies for sustainable fruit growing As societal pressure is on agriculture to reduce and streamline its use of the water resource, ecophysiological studies are elucidating the mechanisms underpinning the interplay between leaf, fruit and stem water relations, and how these affect photosynthesis and fruit growth. Daily variations in water potentials of these organs are involved (in different manners for different species) in the process of fruit growth but, more interestingly, the possibility arises of manipulating the gradients between these potentials that occur during the day. This would enhance the fruit capacity to attract dry matter and water, which are needed to grow, while saving water. Also, current ecophysiological studies are showing that

reductions of up to 50% of irrigation volumes (as determined by FAO coefficient-based scheduling models) can be tolerated without changes in yield and fruit quality of pear (Corelli Grappadelli et al, unpublished). The limit to which these reductions may be taken can be determined by a complex analysis bringing together leaf fluorescence, photosynthesis, leaf, fruit and tree water relations data. Learning to integrate these parameters into ready-to-use knowledge is a challenge for future research. Likewise, information on the daily dynamic of tree vascular flows will pave the way to a novel concept of Regulated Deficit Irrigation, whose time scale will no longer be a seasonal one, but which will be applied daily. Precision fruit growing As increasingly sensor development and ecophysiological knowledge allow to devise novel technologies that can help the grower improve the efficiency of his operation and the quality of the production, integration of the flow of data available into tools that maximize the precision of orchard management is a must. Precision fruit growing is already happening, and it will become the basis for exploitation of the natural resources that are available to the grower and will help reduce the carbon and water footprint of orchards. The physiology of fruit growth has led to the development of predictory models that are already employed commercially by apple and pear growers in Italy [41]. It is easy to see that the future will bring a host of improvements in all stages of orchard management and product handling: from site-specific fertilizer and pesticide application, water management, differential harvests and post-harvest handling. CONCLUSIONS Ecophysiology has been coming a long way, and ecophysiology of fruit trees has claimed a stake within horticultural disciplines for more than the last fifty years, gaining a reputation as a Science that lends itself naturally to produce knowledge amenable to transfer and innovation uptake by growers. It has accompanied the evolution of orchard and tree management over

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the years, and will in the future provide new tools that will continue to enhance the capacity of the growers to improve the sustainability of their operations, while also improving their production of high quality fruit. REFERENCES [1] Barritt, B.H., 1992. Hybrid tree cone orchard system for apple. Acta Hort., 322: 87-92. [2] Byers, R.E., Yers, R.E., Lyons, C.G., Yoder, K.S., 1985. Peach and apple thinning by shading and photosynthetic inhibition. J. Hort. Sci., 60: 465-472. [3] Cain, J.C., 1971. Effects of mechanical pruning of apple hedgerows with a slotting saw on light penetration and fruiting. J. Amer. Soc. Hort. Sci., 96: 664-667. [4] Chow, W.S., Aro, E.M., 2005. Photoinactivation and mechanisms of recovery. In: Wydrzynski, T., Satoh, K., (Eds.) Photosystem II: the light driven water:plastoquinone oxidoreductase. Advances in Photosynthesis and Respiration, Vol. 22 Dordrecht, The Netherlands: Springer, p. 627-648. [5] Corelli Grappadelli, L., Sansavini, S., 1989. Light interception and photosynthesis related to planting density and canopy management in apple. Acta Hort. 243: 159-174. [6] Corelli, Grappadelli L., Lakso, A. N., Flore, J.A., 1994. Early season patterns of carbohydrate partitioning in exposed and shaded apple branches. J. Amer. Soc. Hort. Sci., 119: 596-603. [7] Corelli Grappadelli, L., Ravaglia, G. and Asirelli, A., 1996. Shoot type and light exposure influence carbon partitioning in peach (Prunus persica L. (Batsch)) cv ‘Elegant Lady’. J. Hort. Sci. 71: 533-543. [8] DeJong, T.M., Grossman, Y.L., 1995. Quantifying sink and source limitations on dry matter partitioning to fruit growth in peach trees. Physiol. Plant. 95: 443-445. [9] Doll, P., 2002. Impact of climate change and variability on irrigation requirements: A global perspective. Climatica Change, 54: 269-293. [10] Giuliani, R., Nerozzi, F., Magnanini, E., Corelli Grappadelli, L., 1997. Influence of environmental and plant factors on canopy photosynthesis and traspiration of apple trres. Tree Physiol., 17: 637-645. [11] Heinicke, D.R., 1966. The effect of natural shade on photosynthesis and light intensity in 'Red Delicious' apples trees. Proc. Amer. Soc. Hort. Sci., 88: 1-8. [12] IPCC 2007. Contribution of Working Group II to the Fourth Assessment Report. Parry, M.L., Canziani, O.F., Palutikof, J.P., van der Linden, P.J., Hanson, C.E. (Eds.) Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA. [13] Jackson, J.E., 1967. Variability in fruit size and colour within individual trees. Ann. Rep. E. Malling Res. Station for 1966: 110-115. [14] Kunz, A., Blanke, M.M., 2011. Effects of global climate change on apple “Golden Deliciuos phenology - Based on 50 years of meteorological and phenological data in Klein-Altendorf. Acta Hort., 903: 1121-1126.

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