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Understanding environmental factors and source–sink relationships controlling root growth is critical to understanding how plants may adapt to a changing climate, as well as being essential to efficient agricultural management of woody crops. Although it has been demonstrated that a substantial fraction of a plant's carbohydrate supply can be allocated below ground (Lambers, 1987; Jackson et al., 1997), greater knowledge of the timing of root growth and death and factors regulating this timing is crucial to understanding how plants function in the environment. It is recognized that internal carbon demands in plants (endogenous factors) should interact with environmental factors (exogenous factors) to regulate seasonal changes in root systems (e.g. Tierney et al., 2003). However, our current understanding of how endogenous or exogenous factors regulate root dynamics is limited, particularly under field conditions.
There is particularly limited understanding of how plants balance carbon allocation among different tissues. Although ideas such as optimization theory suggest that plant carbon will be deployed to those absorptive tissues whose resource acquisition most limits plant growth (e.g. Bloom et al., 1985), certain carbon sinks within a plant, such as reproductive organs, demand substantial carbon even though they are not effective resource-acquiring organs. In particular, reproductive organs and roots are often considered to compete for plant carbohydrates (Hansen, 1977). For example, leaf and fine root recovery in response to canopy removal was at the expense of fruit production (Eissenstat & Duncan, 1992). However, there can be trade-offs between reproductive and below-ground allocation, with high reproductive allocation reducing below-ground allocation (Palmer, 1988; Forshey & Elfving, 1989; Rosecrance et al., 1996 and citations therein; Berman & DeJong, 2003). Even in young plants during establishment, high reproductive allocation can decrease below-ground allocation (McLean et al., 1992; Schreiner, 2003). It is unclear, however, how trade-offs in reproductive and root allocation might interact with below-ground resource limitations.
Carbon allocation of woody plants is complicated by their capacity for storage, which is a necessary part of their perennial life strategy for dealing with fluctuations in growing conditions. Woody plants with alternate-year mast cycles store resources to be used in alternate years (Rosecrance et al., 1998). Mild water stress can decrease vegetative shoot allocation without affecting reproductive allocation (Dry et al., 2001; Bryla et al., 2003). Consecutive years of stress, however, could certainly lead to strong negative effects if carbon reserves are debilitated and never replenished. The balance among shoot, root and reproductive growth with resource limitations poses challenging but interesting issues.
Water availability interacts with root growth in a complex fashion. When soil moisture is high and aeration is adequate, root growth can be rapid owing to the abundance of water and lower soil impedance typical at higher soil water contents (reviewed by Richards, 1983). Moderate soil water stress can also enhance root growth, shifting allocation below ground to reduce water limitation for overall plant growth (Freeman & Smart, 1976; Richards, 1983; van Zyl, 1984; Bloom et al., 1985). Even partial drying of root systems can lead to decreased vegetative shoot allocation (Dry & Loveys, 1999). Shoot growth may be more strongly affected by water limitations than is reproductive growth, which could cause carbohydrate reserves to be allocated for reproductive and root growth. Under severe soil moisture stress, however, limited root growth may occur (van Zyl, 1984) because of very low soil moisture availability and high soil impedance (Taylor & Gardner, 1963; Cornish et al., 1984).
Whereas several environmental factors are known to affect root production under field conditions (e.g. Tierney et al., 2003), environmental factors are seldom examined along with seasonal changes in plant carbon balance. Portions of the balance between shoot and root growth and timing of root growth are clearly under genetic control and are part of the life history strategy of plants (Oleksyn et al., 2000). However, most studies of root dynamics have not been able to address both internal and environmental factors. Few studies of below-ground carbon allocation and timing of root growth and death have been of sufficient length to discern relative strengths of endogenous and exogenous factors affecting root dynamics under varying weather conditions. A notable exception was the study by Norby et al. (2004), which found the carbon balance of woody plants to be very responsive to elevated CO2 over 6 yr. Sweetgum plantations more than doubled root production under elevated CO2 while root mortality remained constant, effectively increasing the size of standing root populations. Long-term field studies are needed to discern such effects, which can be variable from year to year.
In its native range in the north-eastern USA, Vitis labruscana grows vigorously, sustaining high yields, and is typically grown on its own root system, unlike many wine grape varieties, which are grafted on rootstocks. In the wild state, grape vines allocate resources mostly to vegetative growth, especially in the shady understory, with large allocation to reproduction only when exposed to full sun (Possingham, 1994). In most viticultural production systems, pruning of up to 90% of the cane (dormant shoots) during the winter season is used to control above-ground vegetative growth, to reduce shading of the fruit and flower buds, and to restrict high reproductive allocation that may stress vines (Possingham, 1994). Minimal canopy removal has recently increased in popularity for native US grapes, resulting in larger early-season vine canopies but similar final canopy sizes and greater reproductive allocation compared with heavily pruned vines. These viticulture systems thus provide the opportunity to examine root dynamics in response to different patterns of above-ground growth in woody plants with intense competition for carbon between vegetative and reproductive organs.
Because patterns of root population dynamics and distribution in the soil profile have rarely been described in relation to shoot phenology and seasonal patterns, our objective was to examine the basic dynamics of root population development over several seasons in a reproductive woody plant with strong trade-offs between vegetative and reproductive growth. We examined root production, pigmentation, mortality and distribution in the soil profile of mature Concord grapevines (V. labruscana) under treatments of heavy and minimal dormant-season cane pruning, with and without irrigation. Treatments were ongoing for 6 yr before the study, ensuring that the vines were equilibrated to the treatments. Root dynamics were observed over four years that varied in rainfall, allowing the effects of fruit production on root dynamics to be assessed under different environmental conditions. We tested the hypotheses that: (1) compared with heavy pruning, minimal pruning promotes early-season root development corresponding to the earlier canopy development under minimal pruning; (2) nonirrigated vines produce more roots at deeper depths in dry years than vines receiving supplemental irrigation, owing to water being more available at deeper depths in dry years; (3) amongst the four treatments, vines exposed to minimal pruning and no irrigation produce the fewest roots, owing to their greater reproductive allocation; and (4) root production is inversely related to reproductive allocation because carbon allocated for reproduction limits the carbon available for root growth.
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We found partial support for our hypotheses on factors affecting root production in Concord grape. Minimal pruning promoted earlier spring root development, which coincided with the earlier canopy development of minimally pruned vines compared with those heavily pruned. Size of root populations among the pruning and irrigation treatments of vines fluctuated between years and different times in the season, governed by endogenous and as well as exogenous factors at various times. Compared with minimal dormant pruning, we found that vines under heavy pruning produced fewer fine roots. Irrigation allowed more root production in dry years and affected the vertical distribution of roots in the soil profile. Heavy reproductive growth was generally associated with lower starch reserves in woody roots, implying that stored reserves may have been used for reproductive growth. In the latter part of the season, few roots were produced once reproductive development reach stages of high carbon demand on the vines. Across different years, heavy reproductive growth in a given year was associated with higher fine root production in the early part of the following year, indicating that greater reproductive allocation did not entirely hamper allocation to roots.
Environmental cues may be part of a signal for initial root production (Fitter et al., 1999; Tierney et al., 2003) but at least a portion of root production appears to be regulated by endogenous factors, possibly linked to photosynthetic supply. Whereas spring root production in all treatments was initiated around the time of bud break (Fig. 3), root flushing generally occurred more quickly in minimally pruned vines (Fig. 2a), corresponding to their faster canopy development (Fig. 1). Furthermore, within pruning treatments (and therefore independent of canopy development), we found additional evidence of endogenous control on root production with treatments that had larger reproductive allocation allocating more resources to root production in the early season of the following year. Biological reasons for increasing allocation below ground could include the facts that: (1) when vines grow vigorously and support heavy reproductive growth, they may also be able to support more root growth; (2) large reproductive allocation may have required more water and nutrients so that in periods following heavy reproductive growth, vines may have been stimulated to increase allocation to roots, which acquire water and nutrients; or (3) after a season of heavy reproductive growth when vines may not have been able to allocate many resources to roots, vines may have increased allocation to roots to make up for limited allocation during the prior period. Although vines with large reproductive growth had lower starch reserves in roots at the end of one season, increased root production in the early portion of the following year may have still been supported by starch reserves, which were low but not depleted, and by current photosynthates. Research tracking carbohydrate allocation with radioactive isotopes has demonstrated that root growth can be supported by current photosynthate (e.g. Thompson & Puttonen, 1992). Although optimization theory suggests that plants selectively allocate resources to acquire a limiting resource, shifts in allocation may only occur at times of the year, such as the early season, when strong competition from reproductive sinks are not present.
The internal carbon balance of the vines may have interacted with irrigation effects, leading to a diminished white root population in minimally pruned vines after two dry years. Minimally pruned vines, which had greater reproductive allocation than heavily pruned vines, did not have reduced capacity to produce roots in a single dry year following a wet year, but after two consecutive dry years, capacity for root production was diminished. Total root populations in minimally pruned vines without irrigation were still greater than those of heavily pruned vines in the second dry year, owing to minimally pruned vines having a large number of brown roots (Fig. 2). However, the metabolic activity of brown roots is low compared with white roots (Comas et al., 2000).
Both endogenous and exogenous factors may have been responsible for limiting root growth during dry years. First, the second dry year (1999) had more intense drought than the first, which likely limited all root production without irrigation in the dry part of the season. Root production in dry conditions could be retarded owing to environmental conditions such as the soil being too dry to allow for root penetration or carbon limitation for root growth under these conditions. While photosynthesis is often reduced under dry soil conditions and could lead to carbon limitations on root growth, root respiration and growth are also greatly reduced, often leading to an increase of starch reserves in plants experiencing drought (Bryla et al., 1997). Root growth of woody plants in climates with seasonal water patterns is often limited at dry times in the season when water is not available (e.g. Katterer et al., 1995). Second, in 1999, reproductive allocation was 70 and 30% higher for heavily pruned and minimally pruned vines than in 1998, which, combined with reduced photosynthesis, may have greatly limited supply of current photosynthates for root growth. The delay in root production in nonirrigated vines during the wet spring of 2000 when environmental conditions should have been optimal for root growth might be indicative of carbon stress in vines in nonirrigated treatments after two dry years. Thus, it appears that a combination of factors may have limited root production in nonirrigated vines in dry years, with soil impedance possibly physically restricting root production in dry soil layers, and reduced photosynthesis eventually leading to limiting carbon availability for root growth.
Root lifespan affects standing populations of roots as much as root production. We had previously reported on the effects of pruning and irrigation on root lifespan over this 4-yr period (Anderson et al., 2003). Irrigation did not affect root lifespan in dry years but slightly decreased root lifespan in wet years. Vines may have retained roots longer in years when root production was limited by dry soil and more readily shed roots selectively in wet years of high root production. Compared with heavily pruned vines, minimally pruned vines had longer-lived roots in wet years but shorter-lived roots in dry years, when minimally pruned vines may have been more stressed (Anderson et al., 2003). Because root population sizes differ between wet and dry years, these interactive effects of pruning and irrigation on root lifespan suggest an intricate interplay between root production and lifespan.
Optimization theory would suggest that nonirrigated vines would have higher allocation to roots than irrigated treatments if plants maximize resource acquisition by allocating more resources to tissues acquiring limiting resources (e.g. Bloom et al., 1985). There was greater stimulation in early-season root production after heavy reproductive growth in the previous year in nonirrigated vines of both pruning treatments (Fig. 7), possibly supporting the optimization theory. However, we did not find that nonirrigated vines had the largest root populations, possibly owing to physical limitations on root production from the soil environment under drought conditions. Nonetheless, as a fraction of net photosynthesis, relative allocation may have increased in nonirrigated vines even though we did not detect any increase in absolute root allocation.
While acknowledging plant control of root production and mortality, soil temperature is widely recognized as an important environmental cue for timing of root dynamics (Lyr & Garbe, 1995; Tierney et al., 2003; Majdi & Ohrvik, 2004). Root production can be restricted when soil temperatures are low in the early spring and late fall. In grape, root growth generally occurs when temperatures are above 6°C and is optimum around 30°C, which is similar to many other temperate plants (reviewed by Richards, 1983). Root production in some woody species has been observed to occur continuously deeper in the soil profile while slowing at shallow depths as the season progresses (Lyr & Hoffmann, 1967). Soil temperatures fluctuate more widely at shallower than deeper depths; thus, soil temperature as a cue for root production is a complex signal affected by depth in the soil profile. Because carbon supply and sinks in a plant change over a season, soil temperature probably only exerts strong effects on root production at soil temperature extremes (e.g. below 10°C and above 35°C) (Richards, 1983; B. Huang, A.N. Lakso & D.M. Eissenstat, unpublished data).
In our study, seasonal production of roots appeared to be governed by a balance of both endogenous and exogenous factors. There was little evidence that either root production or root standing populations exhibited a consistent bimodal pattern, as reported previously for grape in more Mediterranean-type climates (van Zyl, 1988; Mullins et al., 1992). Rather, root production was consistently unimodal for all treatments in wet years and irrigated treatments in dry years but varied in nonirrigated treatments in dry years. Bimodal root production in grape, similar to many temperate woody plants, typically has a large peak in the spring and a secondary peak in the fall (e.g. Mullins et al., 1991). For example, in South Africa, root growth of Colombar/99R exhibits one peak at flowering and another peak at harvest (van Zyl, 1988). In this study as well as ours, root production tapered during fruit ripening. The lack of root flushes in fall in our system may result from the relatively short season, which ends very quickly following harvest as compared with other grape-producing regions.
In conclusion, our study along with others illustrates that the periodicity of root flushes may be jointly regulated by exogenous and endogenous factors: warming temperatures, moisture availability and carbohydrate supply from the shoot triggering root growth in spring; soil moisture limitations and competing carbon sinks restricting root growth in summer; and, in fall, moisture availability and carbohydrate supply from the shoot following harvest, triggering root growth as long as vines do not go immediately into dormancy. Our detailed examination of root production in Concord grape indicated that timing and quantity of root production was closely associated with canopy development when environmental conditions were favorable. There was little consistency in timing, however, of either peak root production or peak root standing populations from year to year, possibly owing to interactions between the carbon balance in the vines and climatic conditions. Simple predictions of timing of root production or standing population with shoot development, consequently, may not be possible. This study also illustrates the need for multiple years of root observations under field conditions to thoroughly investigate patterns of root dynamics associated with plant carbon balance or climatic conditions; only by understanding year-to-year variation can we interpret the relative strengths of endogenous and exogenous factors.