A Review of Elevated Atmospheric CO2 Effects on Plant Growth and Water Relations: Implications for Horticulture

Empirical records provide incontestable evidence for the global rise in carbon dioxide (CO2) concentration in the earth’s atmosphere. Plant growth can be stimulated by elevation of CO2; photosynthesis increases and economic yield is often enhanced. The application of more CO2 can increase plant water use efficiency and result in less water use. After reviewing the available CO2 literature, we offer a series of priority targets for future research, including: 1) a need to breed or screen varieties and species of horticultural plants for increased drought tolerance; 2) determining the amount of carbon sequestered in soil from horticulture production practices for improved soil water-holding capacity and to aid in mitigating projected global climate change; 3) determining the contribution of the horticulture industry to these projected changes through flux of CO2 and other trace gases (i.e., nitrous oxide from fertilizer application and methane under anaerobic conditions) to the atmosphere; and 4) determining how CO2-induced changes in plant growth and water relations will impact the complex interactions with pests (weeds, insects, and diseases). Such data are required to develop best management strategies for the horticulture industry to adapt to future environmental conditions. The level of CO2 in the atmosphere is rising of this research has focused on agricultural and attributed to competitive inhibition of photoat an unprecedented rate, has increased from forest species with limited work on specialty respiration by CO2 and the internal CO2 con­ ;280 ppm at the beginning of the industrial crops associated with horticulture. Horticulture centrations of C3 leaves (at current CO2 levels) revolution (;1750) to ;380 ppm today, and is is a diverse industry (encompassing many small being less than the Michaelis-Menton constant expected to double preindustrial levels somebusinesses) that impacts the landscape of both of ribulose bisphosphate carboxylase/oxygenase time during this century (Keeling and Whorf, rural and urban environments and has an eco(Amthor and Loomis, 1996). Although in­ 2001; Neftel et al., 1985). This global rise can nomic impact of $148 billion annually in the creased photosynthesis under elevated CO2 be primarily attributed to fossil fuel burning United States (Hall et al., 2005). We will atenhances growth for most plants, summaries and land use change associated with industrial tempt to discuss the effects of the rise in atmohave consistently shown that this increase and/or population expansion (Houghton et al., spheric CO2 concentration on plant growth and varies for plants with a C3 (33% to 40% in­ 1990). This rise, along with other trace gases, water relations with a focus toward implications crease) versus a C4 (10% to 15% increase) is widely thought to be a primary factor drivfor horticultural production systems with sugphotosynthetic pathway (Kimball, 1983; Prior ing global climate change (IPCC, 2007). Aside gestions for future research areas. et al., 2003). from the debate on anthropogenic-driven climate Given that most horticulture species have change, vegetation will be directly impacted and a C3 pathway, it is expected that they will PLANT GROWTH research has shown that plants respond posishow similar responses to elevated CO2. Early tively to elevated CO2 (Amthor, 1995). Most Carbon dioxide links the atmosphere to work (Cummings and Jones, 1918) demonthe biosphere and is an essential substrate for strated that both vegetable and flower crops photosynthesis. Elevated CO2 stimulates phobenefited from above ambient concentrations Received for publication 3 Sept. 2010. Accepted tosynthesis leading to increased carbon (C) upof CO2; both cyclamens and nasturtiums for publication 6 Oct. 2010. take and assimilation, thereby increasing plant showed increased dry weight and greater This work was supported by the USDA-ARS, growth. However, as a result of differences in flower yield when exposed to elevated CO2. Floriculture and Nursery Research Initiative. CO2 use during photosynthesis, plants with a Since this early work, others have shown that We thank Barry Dorman for technical assistance. C3 photosynthetic pathway often exhibit greater ornamental species respond positively to eleThis paper was part of the colloquium ‘‘Water growth response relative to those with a C4 vated levels of CO2 (Davis and Potter, 1983; Management and Plant Performance in a Changing pathway (Amthor, 1995; Amthor and Loomis, Gislerød and Nelson, 1989; Mattson and Climate’’ held 4 Aug. 2010 at the ASHS Confer­ 1996; Bowes, 1993; Poorter, 1993; Rogers Widmer, 1971; Mortensen, 1987, 1991; ence, Palm Desert, CA, and sponsored by the Water et al., 1997). The CO2-concentrating mechaMortensen and Gislerød, 1989; Mortensen and Utilization and Plant Performance in a Changing Climate (WUM) Working Group. nism used by C4 species limits the response to Moe, 1992; Mortensen and Ulsaker, 1985). In To whom reprint requests should be addressed; CO2 enrichment (Amthor and Loomis, 1996). fact, increasing the concentration of CO2 in e-mail [email protected]. For C3 plants, positive responses are mainly glasshouses is an economically efficient HORTSCIENCE VOL. 46(2) FEBRUARY 2011 158 method of enhancing growth of ornamental and vegetable crops (Mastalerz, 1977; Mortensen, 1987). In addition to stimulating photosynthesis and aboveground growth, elevated CO2 can alter C partitioning/allocation. Increased C supply from elevated atmospheric CO2 can preferentially induce the distribution of photosynthate belowground (Ceulemans and Mousseau, 1994; Lekkerkerk et al., 1990; Prior et al., 1997; Rogers et al., 1994). In many cases, the largest proportion of the extra biomass produced under elevated CO2 is found belowground (Rogers et al., 1994; Wittwer, 1995), often resulting in increased root-to-shoot ratio (Rogers et al., 1996). This is not surprising in that plants tend to allocate photosynthate to tissues needed to acquire the most limiting resource (Chapin et al., 1987); when CO2 is elevated, the most limiting resource becomes water or nutrients. Although less studied than aboveground response, plants often show increased rooting under CO2 enrichment (Chaudhuri et al., 1986, 1990; Del Castillo et al., 1989; Rogers et al., 1992). In addition to this early work with plants in containers, increased rooting has also been observed in the field using both open-top field chambers (OTC) and free-air CO2 enrichment systems (FACE). Elevated CO2 increased dry weight of root systems for both soybean (44%) and sorghum (38%) growing in OTC (Prior et al., 2003). Prior et al. (1994) also found increases in cotton fine roots (dry weight and length) under FACE and that these plants had proportion­ ately more of their roots allocated away from the row center. Furthermore, Prior et al. (1995) reported that these FACE cotton plants had larger taproots and increases in the number and size of lateral roots. The development of more robust root systems in CO2-enriched en­ vironments may allow for greater carbohydrate storage and infers greater exploration of the soil for resources such as water and nutrients to meet plant growth needs during periods of peak demand such as boll development and filling. In addition to increases in rooting, coloni­ zation of roots with mycorrhizae (the symbi­ otic association of plant roots with fungi) has been shown to increase under elevated CO2 (Norby et al., 1987; O’Neill et al., 1987; Runion et al., 1997). Mycorrhizae increase nutrient uptake by their host plants (Abbott and Robson, 1984), provide additional water to plants through hyphal proliferation in soil (Luxmoore, 1981), and protect roots from path­ ogenic microorganisms (Marx, 1973). Because horticultural plants are generally grown in containers without resource limita­ tions (i.e., water and nutrients), increased root growth or mycorrhizal colonization may not become critical for survival and growth until after outplanting into the landscape. However, as a result of limited rooting space, growth in containers has been shown to dampen the re­ sponse to CO2 enrichment (Arp, 1991). For plants to use a higher level of atmospheric CO2, they must have a means of storing the additional carbohydrates produced. We have shown that plants with a tuberous or woody root system HORTSCIENCE VOL. 46(2) FEBRUARY 2011 tend to respond to CO2 enrichment to a greater degree than plants with smaller or more fibrous root systems (Rogers et al., 1994; Runion et al., 2010). The limited rooting volume experienced by plants growing in containers may help ex­ plain the fact that increased growth of horticul­ tural species under elevated CO2 is sometimes slightly lower than that generally observed for other C3 plants, falling in the range of 15% to 25% (Mortensen, 1991, 1994). Nonetheless, the increased biomass production under high CO2 should be advantageous for horticultural plants in that they should attain a marketable size more rapidly. PLANT WATER RELATIONS In addition to the effects of CO2 on photo­ synthesis and C allocation mentioned, elevated CO2 can impact growth through improved plant water relations (Rogers and Dahlman, 1993). In fact, most plants (both C3 and C4 species) exhibit improved plant water re­ lations. Elevated CO2 slows transpiration by inducing the partial closure of leaf stomatal guard cells (Jones and Mansfield, 1970). Studies in growth chambers and glasshouses have shown that elevated CO2 reduces tran­ spiration for both C3 (Allen et al., 1994; Jones et al., 1984, 1985; Pallas, 1965; Prior et al., 1991; Valle et al., 1985) and C4 (Chaudhuri et al., 1986; Pallas, 1965; Van Bavel, 1974) plants. Dugas et al. (1997), using stem flow gauges under actual field conditions, also showed that whole-plant transpiration was reduced under elevated CO2 for both a soybean (C3) and a sorghum (C4) crop. This reduction in transpiration, coupled with increased photosynthesis, can contribute to increased water use efficiency (WUE = the ratio of carbon fixed to water transpired), which has often been reported (Baker et al., 1990; Morison, 1985; Sionit et al., 1984). In fact, Kimball and Idso (1983) cited 46 obser­ vations that cumulatively showed that tran­ spiration would be lowered by an average of 34%, which, coupled with an economic yield enhancement of 33% (over 500 observations), suggested a doubling of WUE for a doubling of CO2 level. From a physiological standpoint, increased WUE may represent one of the most significant plant responses to elevated CO2 (Rogers et al., 1994). Plants with a C4 photosynthetic pathway show a smaller response to elevated CO2 than plants with a C3 pathway. However, both C3 and C4 plants show reduced transpiration under elevated CO2. Therefore, WUE should be primarily controlled by transpiration in C4 plants, whereas both are important in C3 plants. This was demonstrated by Acock and Allen (1985) using data from Valle et al. (1985) and Wong (1980). In a more recent long-term field study, similar calculations showed contribu­ tions of 74% and 26% (for photosynthesis and transpiration, respectively) in soybean com­ pared with respective contributions of 42% and 58% in sorghum (Prior et al., 2010a). Although photosynthesis still dominated WUE increase in C3 soybean, relative contributions of the two processes were more similar for C4 sorghum than that reported by Acock and Allen (1985). Given the fact that elevated CO2 can reduce transpiration, it has been suggested that this might partially ameliorate the effects of drought (Bazzaz, 1990) and allow plants to maintain increased photosynthesis. This has frequently been observed (Acock and Allen, 1985; Gifford, 1979; Goudriaan and Bijlsma, 1987; Nijs et al., 1989; Rogers et al., 1984; Sionit et al., 1981; Wong, 1980); however, it should be noted that much of this work was conducted in growth chambers and glasshouses using plants growing in containers. Working with container-grown soybean in field OTC, Prior et al. (1991) reported that, at elevated levels of CO2, xylem pressure potential of water-stressed plants was equivalent to that of adequately watered plants, indicating ame­ lioration of drought stress. It has been suggested that in more natural environments, although instantaneous WUE is increased, whole-plant water use may be differentially affected as a result of increased plant size. Allen (1994) reported that larger plant size [higher leaf area index (LAI)] counterbalanced the reduction in water use, offsetting enhanced WUE. Jones et al. (1985) showed that, although elevated CO2 increased WUE for plants with both a high and a low LAI, this increase was greater for plants with a lower LAI. Working with longleaf pine grow­ ing in large (45 L) containers, we found that nitrogen (N) availability was also an important factor affecting the interaction of WUE and plant water stress (Runion et al., 1999). Long­ leaf pine seedlings grown with adequate N grew larger under elevated CO2, resulting in increased whole-plant water use and increased water stress despite increased WUE. Seed­ lings grown with limited N did not exhibit a growth response to elevated CO2, so the in­ creased WUE resulted in decreased whole-plant water use and reduced stress. In addition to improved plant water re­ lations, elevated CO2 can also affect water movement through the landscape. Water in­ filtration can be increased and sediment loss through runoff can be decreased in high CO2 environments (Prior et al., 2010b). These im­ provements can result from increased plant rooting (as noted previously) and from changes in soil physical properties. Elevated CO2 can increase soil C, aggregate stability, and hy­ draulic conductivity and decrease soil bulk density (Prior et al., 2004). These improve­ ments in soil/water relations will be particu­ larly important for horticultural plants in the landscape. Water is also a crucial resource in many horticultural production facilities and its con­ servation is becoming an increasingly im­ portant issue. The fact that elevated CO2 can increase plant WUE (Rogers et al., 1994) may indicate that plants could be watered less frequently as CO2 levels continue to rise. However, because these plants are generally grown with optimal nutrients, elevated CO2 may increase plant size to a point where water­ ing frequency will need to be maintained at current levels or even increased. This interaction