Short-period changes in weather conditions affect xylem, but not phloem flows to young kiwifruit (Actinidia deliciosa) berries

Abstract

Weather conditions are known to affect many physiological parameters like canopy gas exchanges, tree water relations and fruit growth. However, their effects may be different depending on plant species and developmental stage. This study investigates the effects of sudden weather worsening on the daily dynamics of kiwifruit berry growth, at different times during the season. Phloem, xylem and transpiration flows to/from the berry were continuously monitored for several days at about 5, 9, 11 and 15 weeks after full bloom (WAFB), on two consecutive years, while air temperature, relative humidity, solar radiation and rain were simultaneously recorded. From these data vapour pressure deficit (VPD) was also calculated. For each period considered, the daily amounts and the daily patterns of kiwifruit berry relative growth rate (RGR) and vascular flows were compared between two subsequent days having high (HVPD) and low (LVPD) mean VPDs, respectively. During all periods, daily water exchanges were linearly related to VPD although these relationships showed decreasing slopes during the season. At 5 and 9 WAFB daily and hourly rates of xylem and transpiration flows were highly reduced by LVPD conditions, while phloem flow was not affected by such changes during the whole season. Also, LVPD conditions affected the typical daily fluctuations in the berry RGR by reducing its morning shrinkage and slowing down its afternoon growth rates. This study shows how in the early stages of kiwifruit berry growth, weather worsening highly reduces the berry water exchanges by xylem and transpiration, but does not affect its phloem imports in the short-period.

Introduction

Fruit growth is the result of complex biophysical and biochemical processes that bring water and dry matter into fruit tissue. Xylem and phloem flows are the main sources for water and dry matter and determine the daily and seasonal increase in fruit weight. However, fruit species like peach (Fishman and Génard, 1998, Morandi et al., 2007a) and kiwifruit (Dichio et al., 2003, Montanaro et al., 2006, Morandi et al., 2010a) loose significant amounts of water through epidermis transpiration, which can determine hourly reductions in fruit weight and thus diameter shrinkages during the day. Usually, fruit water potential is negatively related to fruit transpiration rate, as the higher the tissue dehydration, the lower its hydrostatic pressure and osmotic potential (Nobel, 2005). Therefore, epidermis transpiration can represent an useful tool for the fruit to decrease its water potential and retrieve, by bulk flow, water, carbohydrates and mineral elements from the phloem and xylem streams, which are driven by hydrostatic pressure gradients in the vascular path. However, other fruit species, like apple, require a final, energy-dependent step to import phloem carbohydrates into their tissue (Zhang et al., 2004). In this case, phloem unloading does not depend on phloem-to-fruit water potential gradients (Patrick, 1990, Patrick, 1997), although hydrostatic pressure gradients in the vascular path may still facilitate resources translocation towards the fruit (Münch, 1930). In the case of the peach fruit, on the other hand, at least part of the carbohydrates are unloaded passively; here, phloem flow is enhanced by environmental conditions facilitating epidermis transpiration (Morandi et al., 2010b).

Weather conditions highly affect leaf and fruit water relations: high temperature and low relative humidity increase evapo-transpiration (Nobel, 2005) while leaf stomatal conductance is positively affected by solar radiation (Jarvis, 1976). Water losses may in turn affect leaf and fruit water status, the hydrostatic pressure gradients among different plant organs and, consequently, the vascular flows at whole tree level. Weather conditions can also affect carbohydrate availability for the sinks as the photosynthetic process is highly dependent on light irradiance and can be reduced when photosynthetic active radiation (PAR) is not saturating, as it may occur on cloudy and rainy days (Bohning and Burnside, 1956).

Therefore, the physiological processes underpinning fruit growth are likely to be affected by changes in environmental conditions whose effects may seem to change with the species. In apple, fruit phloem flow was progressively reduced after the application of 90% shading nets to the orchard (Morandi et al., 2011); in peach, fruit phloem and xylem flows were found to be enhanced by higher VPD (Morandi et al., 2010b), whereas in tomato increased VPD reduced fruit xylem inflows due to the lowering of stem water potential, while phloem flow was almost unaffected (Guichard et al., 2005). Modelling of fruit growth is often based on the most important environmental parameters as independent input variables (Fishman and Génard, 1998, Léchaudel et al., 2005), although other factors, like source-sink ratio or resource availability, may have an even more important impact on final fruit weight. Kiwifruit berry is characterized by a first stage of rapid diameter growth followed by a second period of slow growth which lasts until harvest (Gallego et al., 1997, Ferrandino and Guidoni, 1998). This seasonal change is due to anatomical modifications occurring at berry level (Morandi et al., 2010a). As fruit develop, their epidermis conductance to water vapour sharply decreases (Hallett and Sutherland, 2005, Celano et al., 2009) while fruit xylem vessels decrease progressively their conductivity (Morandi et al., 2010a, Clearwater et al., 2012). These changes lead to the progressive seasonal reduction of fruit water exchanges by xylem and transpiration flows (Montanaro et al., 2006, Morandi et al., 2010a). On the other hand, phloem imports on a whole fruit basis remain constant during the season and determine the continuous increase of fruit dry matter content (Morandi et al., 2010a), although it is not yet clear whether kiwifruit phloem unloading is symplasmic or apoplasmic and whether it shifts from one model to the other during the season.

In a previous study, vascular and transpiration flows to kiwifruit berries were quantified, under clear sunny conditions, at different times during the season (Morandi et al., 2010a). Results from this work showed how the typical daily fluctuations in vapour pressure deficit (VPD) highly affect fruit transpiration, but not xylem flow. Indeed, despite this flow is related to fruit transpiration by bulk flow mechanisms, it also depends on water availability in the stem and, unlike transpiration, it does not respond directly to external VPD during the day (Morandi et al., 2010a). Due to the high leaf transpiration rates of this species, some xylem backflows from fruit to leaves can also occur during the morning hours, in response to the decreased stem water potential (Morandi et al., 2010a).

Therefore, it is not clear yet whether a decrease in air VPD due to weather worsening may increase kiwifruit berry xylem inflow, due to a rise in the stem water potential, as occurs in tomato (Guichard et al., 2005), or decrease it, due to the likely increase in fruit pressure potential, which may follow the reduction in berry transpiration. This issue is quite important as it may impact fruit Ca accumulation, which is translocated only via xylem flows.

Similarly to the xylem, the daily pattern of phloem flow seems unrelated to hourly changes in the environmental conditions, although it may indirectly respond to leaf photosynthesis and thus to assimilates availability for translocation, which on their turn might be reduced by cloudy conditions.

As they respond to water potential gradients in the vascular path, vascular flows and thus fruit growth are likely to be affected by sudden weather worsening. The impact of such changes on the fruit growing process might be different depending both on the fruit species and phenological stage, and it might have significant effects on the final fruit quality.

This work builds up from Morandi et al. (2010a), where the daily dynamics of kiwifruit berry growth, vascular and transpiration flows were studied under sunny conditions, at different times during the season. Here, we show how these dynamics respond to short-term changes in weather conditions, and how these responses change with fruit developmental stage.