High temperature reduces the positive effect of elevated CO2 on wheat root system growth

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High temperature reduces the positive effect of elevated CO2 on wheat root system growth Maria Benlloch-Gonzalez a , Rocco Bochicchio b , Jens Berger c , Helen Bramley d,1 , Jairo A. Palta c,e,∗ a Departamento de Agronomía, Universidad de Córdoba, Campus de Excelencia Internacional Agroalimentario, ceiA3, Ctra. Madrid-Cádiz, Km. 396, E-14071 Córdoba, Spain b Dipartimento di Scienze dei Sistemi Colturali, Forestali e dell’Ambiente, Università della Basilicata, viale dell’Ateneo Lucano 10, 85100 Potenza, Italy c CSIRO, Plant Industry, Private Bag No. 5, Wembley, WA 6913, Australia d The UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia e School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia

a r t i c l e

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Article history: Received 5 January 2014 Received in revised form 29 March 2014 Accepted 5 April 2014 Available online xxx Keywords: Wheat root system Elevated CO2 High temperature Rhizo-boxes Climate change

a b s t r a c t Increases in atmospheric carbon dioxide concentration ([CO2 ]) and temperature associated with future climates are expected to affect wheat growth and grain yield. The ability of wheat to adapt to these changes is close related to the response of the root system. The effect of elevated CO2 , high temperature and the interaction elevated CO2 × high temperature (3 ◦ C above the ambient temperature) on the growth and proliferation of the root system of two spring wheat genotypes differing in vigorous growth was evaluated. The breeding line Vigor 18 selected for vigorous shoot and root growth and the commercial cultivar Janz were grown in rhizo-boxes inside specially designed tunnel houses under ambient (390–400 ␮L L−1 ) and elevated CO2 (700 ␮L L−1 ), and ambient and 3 ◦ C above the ambient temperature. Growth and proliferation of the root system was monitored through root mapping. Elevated CO2 enhanced root and shoot biomass, but this positive effect was reduced when plants were grown under high temperature. Total root length was also increased by elevated CO2 , but only when plants were grown under ambient rather than under high temperature. Root growth response to elevated CO2 differed between genotypes; elevated CO2 stimulated root growth in the non-vigorous cultivar Janz, but not in vigorous liner Vigor 18. High temperature reduces the positive effect that elevated CO2 has on root growth and proliferation. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Atmospheric [CO2 ] is steadily increasing and is expected to rise from the current level of ∼384 ␮L L−1 to ∼550 ␮L L−1 by 2050 (Carter et al., 2007). It is predicted that global temperature will increase by 1.5–4.5 ◦ C as well as the frequency heat waves and drought spells (Carter et al., 2007). Increases in [CO2 ] and temperature directly influence the growth, development and grain yield of wheat by increasing rates of photosynthesis and phenological development (Semenov et al., 2012). Special attention has been

∗ Corresponding author at: CSIRO Plant Industry, Private Bag No. 5, Wembley, WA 6913, Australia. Tel.: +61 08 9333 6611; fax: +61 08 9387 8991. E-mail address: [email protected] (J.A. Palta). 1 Present address: Plant Breeding Institute, Faculty of Agriculture and Environment, The University of Sydney, 12656 Newell Highway, Narrabri, NSW 2390, Australia.

paid to the impact of increasing [CO2 ] and temperature on aboveground traits in different crops (Reynolds-Henn et al., 2010; Wertin et al., 2010), but growth and development of the root systems may also be affected (St Clair and Lynch, 2010). Root and shoot growth are so interdependent that one cannot succeed without the other, in fact above-ground growth and biomass yield of most crops are influenced by the capacity of the root system to take up water and nutrients from the soil (Hammer et al., 2009). According to the concept of ‘functional equilibrium’ between shoot and root growth, an increase in atmospheric resources such as CO2 and temperature should increase relative partitioning of resources into roots so that the balance between assimilation of carbon and nutrients is maintained (Brouwer, 1963, 1983). Wheat has a fibrous root system consisting of two parts, the primary and the secondary roots. The primary (seminal) roots are the first to appear after germination. The secondary root system, called adventitious or nodal roots, develops when the plants begin to tiller; they are thicker than the primary roots and usually emerge

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horizontally. When abiotic factors, such as drought, prevent secondary roots from growing, the primary root system can support sufficient plant function to produce some grain (Weaver, 1926). As the root system matures it spreads and branches in parallel with leaf growth, often ceasing by the time of anthesis (Gregory, 2006; Palta and Watt, 2009). The root system has morphological and physiological plasticity in response to different environments, changing its distribution within the soil profile (Drew et al., 1973; Smucker and Aiken, 1992; Feddes and Raats, 2004; Benlloch-Gonzalez et al., 2014). Therefore, knowledge of the root system growth dynamics and architecture may play an important role in crop adaptation to the future climates. Most studies into the impact of increasing [CO2 ] and temperature on root growth and development have focused on the effects of elevated [CO2 ] and high temperature independently. Root growth of most crops is enhanced under elevated atmospheric CO2 (Rogers et al., 1994; Pritchard and Amthor, 2005), often to a greater extent than leaves, stems, and reproductive structures (Norby et al., 1992; Kimball et al., 2002). Crop root systems respond to elevated CO2 differently. For instance, soybean produces more biomass and longer roots (Del Castillo et al., 1989; Rogers et al., 1992), cotton produces heavier roots (Reddy et al., 1994) and in sorghum more roots at all depths of the soil profile has been observed when the aerial parts were exposed to elevated CO2 (Chaudhuri et al., 1986). The growth response of the wheat root system to elevated atmospheric CO2 is variable. For example, some studies have observed a greater root biomass under elevated CO2 (Gifford et al., 1985; Chaudhuri et al., 1990; Acock et al., 1990; Weigel et al., 1994; Barnes et al., 1995; Balaguer et al., 1995) while others have observed hardly any effect (Kendall et al., 1985; Frank and Bauer, 1996; Slafer and Rawson, 1997; Gavito et al., 2001). These contrasting responses to elevated CO2 appear to be related to genotypic differences. Root biomass was reduced in genotypes with vigorous root systems, but it was not affected in restricted tillering genotypes (Benlloch-Gonzalez et al., 2014). Along with an increase in CO2 levels in the atmosphere, air temperature is also expected to increase in the future (IPCC, 2007a,b). Increases are expected in both mean temperature, as well as the frequency of extremely high temperature (IPCC, 2007a,b). Wheat crops will be then exposed to high temperatures, which will have a significant impact on the crop growth, development and grain yield (Farooq et al., 2011). Since wheat above-ground growth and development is isometrically related to below-ground growth (Qin et al., 2012), it is expected that the form and function of the root system to be affected when wheat crops are exposed to high air temperatures. It is generally accepted that wheat biomass increases with increasing air temperature until a threshold optimum temperature is reached (DeLucia et al., 1992). Similar tendencies for root length and branching are accepted (Kasper and Bland, 1992). However, little is known about the growth and proliferation of the wheat root system when plants are grown under temperatures that are higher than the ambient temperatures. Little is known about the interactive effect of elevated [CO2 ] and high temperature on the growth and proliferation of the root system in wheat. It is not clear whether the positive response of shoot biomass to elevated CO2 (Kimball, 1983) will still be enhanced under high temperature or how it will affect root growth and proliferation. Therefore, the aim of this study was to evaluate the effect of elevated CO2 combined with higher mean temperature on the growth of the root system of two spring wheat genotypes contrasting in vigor: a wheat breeding line Vigor 18 selected for vigorous shoot and root growth (Rebetzke and Richards, 1999; Liao et al., 2006; Palta et al., 2011) and the commercial cultivar Janz (Brennan et al., 1991). It was hypothesized that Vigor 18 would demonstrate greater plasticity to the combined effect of elevated CO2 × high temperature and root growth would be stimulated more

than Janz. The two genotypes were grown in rhizo-boxes (Liao et al., 2006) inside specially designed tunnel houses in which CO2 , temperature and irrigation were controlled (Dias de Oliveira et al., 2013). 2. Material and methods 2.1. Plant material Wheat (Triticum aestivum L.) cultivar Janz, a current wheat commercial cultivar widely adapted in southern Australia, and the vigor wheat line Vigor 18 selected for vigorous shoot and root growth by Drs. R. Richard and G. Rebetzke at CSIRO Plant Industry, were grown in glass-walled rhizo-boxes filled to a depth of 1.0 m with soil. The soil was a Gingin dark brown loam soil (Hosking and Greaves, 1936), consisting of 40% brown sand, 40% silt and 20% clay. The pH, measured in a 1:5 suspension of soil in 0.01 M CaCl2 was 5.3–6.1. The soil was put through a 2 mm sieve and then packed to a bulk density of approximately 1.53 g cm−3 . Seeds were germinated on filter paper moistened with deionised water, in covered Petri-dishes, at room temperature for 48 h. Four of the most uniformly germinated seeds were sown in a row close to the glass wall in each rhizo-box when roots were 0.5–1 cm in length. At sowing, on 27 October 2012, the equivalent of 80 kg N ha−1 as urea and 20 kg P ha−1 as amended superphosphate (with Cu, Zn, Mo, S) was mixed into the top 0.1 m of soil in each rhizo-box. The rhizo-boxes were similar to those used by Liao et al. (2006), Palta et al. (2007) and Benlloch-Gonzalez et al. (2014). Briefly, they were constructed from polyvinyl chloride (PVC) and were 0.24-m long, 0.10-m wide and 1.0-m deep, with one glass wall. The glass wall was covered with a black PVC sheet to avoid any light exposure of the roots. The rhizo-boxes were placed on steel stands at an angle of 30◦ and spaced 0.05 m apart. An adjustable sleeve made from Isofax1260 ◦ C high temperature insulation blanket (25 mm thick, 96 kg m−3 density; Unifrax Co., Niagara Falls, New York, USA) was used to wrap each rhizo-box to prevent temperature exposure of the soil in the rhizo-boxes. The plants in each rhizo-box were grown in four tunnel houses in the field at the University of Western Australia Research Station at Shenton Park, Western Australia (WA). Each rhizo-box (four plants) served as a replicate and there were three replicates per each treatment and genotype (24 rhizo-boxes). 2.2. Tunnel houses The tunnel houses were similar to those used by Dias de Oliveira et al. (2013). Briefly, each tunnel house, 10 m long × 2.5 m wide × 2.5 m tall, consisted of a steel frame covered with a double sheet of F-clean greenhouse film (200 ␮m) (AGC Chemicals Americas, Inc., Exton, PA, USA). This film allows 96% light transmission, is impermeable to CO2 , and inflation between double walls insulates against external temperature. Air flow through each tunnel was provided by a CPD 0454 FHP multi-speed fan (Fantech, Pty, Ltd., Melbourne, VIC, Australia) capable of moving 1333 L s−1 of air. Each fan moves outside air through a cardboard radiator window mounted in the opposite wall of the tunnel. The fan speed was varied continuously with an ACS150 Drive (ABB Inc., New Berlin, WI, USA) to maintain a set temperature inside the tunnel, which was monitored with a TWA 27708 Resistance Thermometer Detector (Technitemp, Instruments and Controls Pty, Perth, WA, Australia) at the end of the tunnel. Certified CO2 gas was pulsed from a gas vessel (BOC Special Gases, Chatswood, NSW, Australia) through a 1.5 m × 15 mm diameter plastic hose connected via a solenoid valve into the inside wall of the cardboard radiator window (inlet stream) of each tunnel. A space of 1 m × 2.5 w × 2.75 h was left free from

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the CO2 injection point to avoid any injection pressure of the CO2 on the plants and to evenly distribute the pulse of CO2 before it passed though the plants in the rhizo-boxes. Fluctuations in CO2 concentration inside each tunnel were prevented by continuous monitoring of CO2 concentration above the plant canopy. Measurements were made using a GAS-CO2 -002-K infrared gas analyser (Gas Alarm System, Sydney, NSW, Australia). These measurements set the rate of the pulse of the solenoid valve so that when the CO2 concentration drops by 1 ␮L L−1 , the solenoid valve opens to let the CO2 enter and re-establish the target concentration, and subsequently closes. Instantaneous spot measurements of CO2 and temperature were conducted throughout the experiment at different spots in each tunnel with an Extech-CO250, portable CO2 temperature, relative humidity Meter-Datalogger (Extech Instruments Co., Townsend West, Nashua, NH, USA) to ensure that there were no gradients in temperature and CO2 concentration inside each tunnel (accurate to ±1 ppm for CO2 , ±0.1 ◦ C for temperature and ±0.1% for relative humidity). The tunnel-system was automatically regulated so that when CO2 uptake by plants increased at high irradiance, the fan speed also increased to control the associated temperature rise and the CO2 injection rate increased to compensate for the diluting effect of the increased air flow. When a tunnel was set to ambient CO2 and temperature, the fan moved air through the tunnel with CO2 concentrations from outside the tunnel between 390 and 400 ␮L L−1 and fan speed was determined by continuously monitoring air temperature outside the tunnel. Temperature and CO2 concentration inside the tunnels were scanned every 5 s, and 30-min averages were stored by an 8-channel data logger (TP488-RT, Amalgamated Instrument Co., Pty, Ltd., Hornsby, NSW, Australia) and visualised with the software WindowsTM Compatible Logging & Live Reading (Amalgamated Instrument Co. Pty Ltd., Hornsby, NSW, Australia). The CO2 injection was maintained 24 h per day. The soil of each tunnel house was irrigated three to four times per week with a reticulation system to maintain soil water content close to field capacity. During the experiment (October–December), each tunnel received 11–12.6 h of daylight, with an average maximum photosynthetic photon flux density (PPFD) inside the tunnels of 1168 ± 13 ␮mol m−2 s−1 , at 1300 h (Fig. 1a supplementary). The average maximum and minimum temperatures inside the tunnels were 25.1 ± 0.27 ◦ C and 13.3 ± 0.32 ◦ C, respectively for the tunnels under ambient temperature and 28.5 ± 0.42 ◦ C and 13.3 ± 0.34 ◦ C for those under high temperature (Fig. 1b supplementary). Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.fcr.2014.04.008. 2.3. Treatments Each tunnel house was set up with a different combination of CO2 and temperature, as follows: 1. Elevated CO2 (700 ␮L L−1 ) and 3 ◦ C above the ambient temperature [ECO2 + HT]. 2. Elevated CO2 (700 ␮L L−1 ) and ambient temperature [ECO2 + AT]. 3. Ambient CO2 (398–401 ␮L L−1 ) and 3 ◦ C above the ambient temperature [ACO2 + HT]. 4. Ambient CO2 (398–401 ␮L L−1 ) and ambient temperature [ACO2 + Ambient T].

3

of white plastic beads. The maintenance of the soil water content in each rhizo-box close to field capacity, while minimizing soil evaporation reduced the effect of different wind speed within the tunnel houses. Although vapour pressure deficit (VPD) was not controlled, it was unlikely to influence our results. The typical diurnal pattern of VPD observed during the experiment (Fig. 1c supplementary) shows that the highest VPD (2.52 kPa) occurred at midday inside the +3 ◦ C tunnels, a value only 0.35 kPa higher than in the ambient temperature tunnels. This small difference is not large enough to generate differences in transpiration rate among the temperature treatments and wheat genotypes (Schoppach and Sadok, 2012). The experiment was finished when six of the twelve longest seminal roots reached the bottom of the box in 50% of the rhizoboxes at 48 days after sowing (DAS). A number of studies have indicated that the form and function of the root system of wheat is altered when the seminal roots grown against the bottom of pots (Townend and Dickinson, 1995; Ray and Sinclair, 1998; Passioura, 2006; Poorter et al., 2012). At 48 DAS when the plants were harvested the flag leaf sheath was extending (Z41; Zadoks scale of cereal development; Zadoks et al., 1974). 2.4. Root mapping At weekly intervals, after the 1-leaf stage (6 DAS) until the end of the experiment (48 DAS), the growth and proliferation of the root system was followed through the glass wall of each rhizo-box (Liao et al., 2006). Each time, the black PVC cover sheet was removed and replaced with a transparent plastic film and all the visible new roots were traced on the transparent film using a waterproof permanent pen. After removal of the transparent film from the glass wall, all the visible new roots were also marked on the glass wall. In this way, it was possible to identify the new root growth at the subsequent measurement time without the need of using different colours for tracking of the roots. The black PVC cover-sheet was then replaced over the glass wall. The transparent film for each mapping day was photographed with a digital camera and the images were analysed for the length of the roots using the computer software WinRHIZO 2008 (model Pro, second version, Regent Instruments Inc., Canada). 2.5. Sampling The above- and below-ground biomass was measured at 48 DAS, when the experiment was harvested. The four plants in each rhizobox were harvested as a single replicate. Plants were harvested by cutting the shoots from the roots at the crown. The number of tillers was recorded and the green leaf area (LA) was measured with a leaf area meter (LI-COR Model LI-3100, Lincoln NE, USA) before being dried at 70 ◦ C for 72 h and then weighed. Immediately after the shoots were harvested, the rhizo-boxes were opened by removing the glass wall and the soil in each box was sampled in 0.2-m sections. The roots in each section were recovered from the soil by repeated sieving on a 1.4-mm sieve to produce a clean sample as described by Liao et al. (2006) and Palta et al. (2007, 2010). After the roots were recovered from a section of the soil, they were placed in paper bags, dried at 70 ◦ C for 48 h and weighed. 2.6. Statistical analysis

Changes in soil water content in the rhizo-boxes were not measured, but before sowing the soil in each rhizo-box was saturated with water and covered with aluminum foil paper and left to drain for 48 h. The rhizo-boxes were watered carefully by hand three to four times per week to ensure the soil was wet while avoiding drainage of excess water. Soil evaporation from each rhizo-box was reduced by covering the soil surface with a 5-cm uniform layer

The four tunnels were located in close proximity, adjacent to each other in the Shenton Park field station, while rhizo-boxes were arranged randomly in blocks in each tunnel (n = 3). Tunnels were treated as separate environments, with blocks nested within environment. The data was analysed using Genstat V13 using ANOVA and linear regression. In all analyses, residual plots were generated

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3. Results The main effects of CO2 , temperature and genotype were often significant. However, the two-way interactions were usually significant in every measured parameter, and were investigated more closely to check whether main effects were meaningful in the light of these interactions. Therefore, the results below report on the interaction when it occurs and main effects only when these are meaningful. 3.1. CO2 × temperature interaction There were no meaningful three-way interactions between temperature, CO2 and genotype, whereas CO2 by temperature interactions were observed in stem dry matter (DM), shoot and root biomass (P < 0.05) (Figs. 1 and 2). Under ambient CO2 there was no effect of temperature on stem DM, shoot and root biomass, but under elevated CO2 stem DM, shoot and root biomass increased under both ambient and high temperature. The increase was much greater under ambient than under high temperature. The response of total traced root length to elevated CO2 was somewhat different (Fig. 3). Root length increased under elevated CO2 and ambient temperature, but there was no response under high temperature. 3.2. CO2 × genotype interaction There were no temperature by genotype interactions (P = 0.110 to P = 0.909) in any above- or below-ground parameter measured. CO2 × genotype interactions were common, occurring in green leaf area (LA), leaf DM, stem DM and the number of tillers (P < 0.05 to P < 0.01) (Table 1). Elevated CO2 had a positive effect on LA, leaf DM and tiller number in the cultivar Janz, but not in the line Vigor 18. Elevated CO2 increased LA, leaf DM, stem DM and the number of tillers in Janz by 68–107% (Table 1). Genotype main effects were also important in some parameters. LA, leaf DM, and the number of tillers were consistently greater in Janz than in Vigor 18 under both ambient and elevated CO2 (Table 1). Stem DM was significantly greater in Janz than in Vigor 18 under elevated CO2 only (Table 1). The effect of CO2 on root biomass and total traced root length was also dependent on the genotype (P < 0.05 to P < 0.01) (Fig. 4).

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to identify outliers, and confirm that variance was common and normally distributed.

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Fig. 2. Shoot biomass (a) and root biomass (b) at 48 DAS (Z41) in wheat plants grown under ambient (390–400 ␮L L−1 ) and elevated CO2 (700 ␮L L−1 ) and ambient temperature and 3 ◦ C above the ambient temperature. Bars indicate means for the interaction CO2 × temperature on shoot and root biomass. Vertical bar represents l.s.d. of means at P < 0.05, n = 3.

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Fig. 1. Stem dry matter accumulation at 48 DAS (Z41) in wheat plants grown under ambient (390–400 ␮L L−1 ) and elevated CO2 (700 ␮L L−1 ) and ambient temperature and 3 ◦ C above the ambient temperature. Bars indicate means for the interaction CO2 × temperature on stem dry matter. Vertical bar represents l.s.d. of means at P < 0.05, n = 3.

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Fig. 3. Total root length (up to 1 m depth) at 48 DAS (Z41) in wheat plants grown under ambient (390–400 ␮L L−1 ) and elevated CO2 (700 ␮L L−1 ) and ambient temperature and 3 ◦ C above the ambient temperature. Measurements were made by root mapping at 6–7 day intervals starting from 6 DAS. Bars indicate means for the interaction CO2 × temperature on total root length. Vertical bar represents l.s.d. of means at P < 0.05, n = 3.

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Table 1 Leaf area (LA), leaf dry matter (DM), specific leaf area (SLA), stem dry weight (DM), tiller number, and above-ground biomass at 48 DAS (Z41) in the non-vigorous cultivar Janz and the vigorous line Vigor 18 grown under ambient (390–400 mL L−1 ) and elevated CO2 (700 mL L−1 ). *P < 0.05, **P < 0.01, ns P > 0.05 for CO2 level × genotype interaction. Genotype

CO2 level

Janz

Ambient Elevated

Vigor 18

Ambient Elevated

CO2 level × genotype LSD (P = 0.05)

Leaf DM (g/plant)

SLA (cm2 g−1 )

Stem DM (g/plant)

Tillers (plant−1 )

Biomass (g/plant)

74.2 124.9

0.37 0.62

202.4 201.2

0.71 1.47

2.9 5.6

1.11 2.25

36.6 44.9

0.17 0.21

211.8 218.9

0.69 0.94

1.2 1.5

1.28 1.78

* 28

* 0.16

ns 18.7

* 0.44

** 1.2

ns 0.71

LA (cm2 )

Elevated CO2 had a positive effect on root biomass and total root length in the cultivar Janz, which increased by 127% and 46%, respectively, whereas no effect was observed in Vigor 18 (Fig. 4a and b). As a result there were large genotypic differences in root 1.4 ACO2

a)

ECO2

Root biomass (g/plant)

1.2

3.3. Changes in root length with time

1.0

Figure 4

Linear regression of root length over time, with CO2 , temperature, and genotype fitted as factors explained 94.3% of the variance (Fig. 5). Root length rates in cultivar Janz increased with elevated CO2 under both ambient (P < 0.001) and high (P = 0.013) temperature (Fig. 5a). The greatest response in root length in Janz occurred under ambient temperature (Fig. 5a). Root extension rates in Vigor 18 increased under elevated CO2 , when plants were grown under ambient temperature only (P = 0.011) (Fig. 5b). There were no differences in root extension rates in Vigor 18 between ambient and elevated CO2 under high temperature (P = 0.725) (Fig. 5b).

0.8 0.6 0.4 0.2 0.0

Total root length (cm/plant)

b)

1000 800

3.4. Changes in root biomass and length with soil depth

600

Nonlinear (exponential) regression of root biomass against soil depth, with CO2 , temperature, and genotype fitted as factors explained 68–92% of the variance (Fig. 6). ANOVA performed for each 20 cm layer of the 1 m soil profile indicated significant interaction of (i) genotype × CO2 in 0–60 cm soil layers (P = 0.02 to P < 0.01) (Fig. 6a) and (ii) CO2 × temperature interaction in 0–40 cm soil layers (P < 0.05) (Fig. 6b). CO2 × genotype interactions were explained by the stronger response of root biomass to CO2 in Janz than in Vigor 18. Elevated CO2 increased root biomass accumulation in the 0–60 cm soil layers in Janz, whereas no effect was observed in Vigor 18. This effect was more marked in the top soil layer (0–20 cm). There were no differences between the two genotypes in root biomass in the top soil layer under ambient CO2 , while under elevated CO2 Janz had greater root biomass than Vigor 18 (Fig. 6a). Below 60 cm of the soil profile there were no differences in any treatment combinations (P = 0.228–0.922). Similar trends were observed for root length with soil depth (P < 0.001; data not presented). CO2 × temperature interactions were explained by the stronger response to CO2 under ambient compared to high temperature (Fig. 6b). In the 0–20 cm of the soil profile a positive effect of CO2 in root biomass accumulation was observed under both ambient and high temperature, albeit the effect was stronger under ambient temperature. In the 20–40 cm soil layer the positive effect of CO2 on root biomass occurred under ambient CO2 only. In deeper soil layers (>40 cm) no effect of CO2 or temperature occurred (Fig. 6b). As observed in the previous interactions, similar trends were observed in root length with soil depth (P < 0.05; data not presented).

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35 30

Root index (g g-1)

biomass under elevated, but not under ambient CO2 . In contrast there were no differences in total traced root length between Janz and Vigor 18 under both elevated and ambient CO2 (Fig. 4b). Elevated CO2 reduced the root index in Vigor 18 by 20%, but had no effect on Janz (Fig. 4c). The root index was consistently greater in Janz than in Vigor 18 both under ambient and elevated CO2 (24% and 43%, respectively) (Fig. 4c).

25 20 15 10 5 0

Janz

V18 Genotype

Fig. 4. Root biomass (a), total root length (b), and root index (c) at 48 DAS (Z41) in the non-vigorous cultivar Janz and the vigorous line Vigor 18 grown under ambient (390–400 ␮L L−1 ) and elevated CO2 (700 ␮L L−1 ) and ambient temperature and 3 ◦ C above the ambient temperature. Bars indicate means for the interaction CO2 × genotype on root biomass, total root length and root index. Vertical bar represents l.s.d. of means at P < 0.05, n = 3.

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DAS Fig. 5. Changes in total root length with time (DAS) in the non-vigorous cultivar Janz (a) and the vigorous line Vigor 18 (b) when grown under ambient (390–400 ␮L L−1 ; ACO2 ; open symbols and elevated CO2 (700 ␮L L−1 ; CO2 ; filled symbols), and ambient temperature AT; squares) and 3 ◦ C above the ambient temperature temperatures (HT; circles) combinations. Measurements were made by root mapping at 6–7 day intervals starting from 6 DAS. Values are the mean of three replicates. The lines shown are linear regressions for CO2 , temperature and genotypes fitted as factors.

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Fig. 6. Changes in root biomass with soil depth down a 1 m soil profile. (a) Effect of CO2 × genotype interaction for Janz (squares) and Vigor 18 (circles) when they were grown under ambient (ACO2 ; open symbols) and elevated CO2 (ECO2 ; filled symbols). (b) Effect of ambient CO2 (ACO2 ; squares), elevated (ECO2 ; circles) and ambient temperature (open symbols) and 3 ◦ C above the ambient temperature temperatures (filled symbols) interaction. Measurements were made 48 DAS. Values are the mean of three replicates. Horizontal bars represent l.s.d. of means at P < 0.05.

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4. Discussion The combined effect of elevated CO2 (700 ␮L L−1 ) with high temperature (3 ◦ C above the ambient temperature) on wheat growth was not dependent on the genotype. Elevated CO2 enhanced shoot and root biomass accumulation under both ambient and high temperature, but the positive effect of elevated CO2 on biomass accumulation was reduced when plants were grown 3 ◦ C above the current ambient temperature. A positive effect of elevated CO2 was also observed on total root length but only when plants were grown under ambient temperature. Hence, high temperature restricted the positive effect of elevated CO2 on shoot and root biomass and root length. The slight effect of elevated CO2 on shoot and root biomass accumulation under high temperature observed in this study is supported by the findings of Mitchell et al. (1993) and Batts et al. (1997) for winter wheat. It is also supported by the findings of Dias de Oliveira et al. (2013) for spring wheat where the combination of elevated CO2 (700 ␮L L−1 ) and 4 ◦ C and 6 ◦ C above the ambient temperature did not enhance biomass and grain yield, but tended to decrease them. The mean maximum temperature inside the tunnel house in which plants were grown under elevated CO2 and high temperature (26.8 ◦ C) was above the optimum for photosynthesis and growth of wheat (20–25 ◦ C; Austin, 1990; Nagai and Makino, 2009) and this may lead to the smaller response to elevated CO2 under high temperature. The slight effect of elevated CO2 on shoot and root biomass and root length under high temperature is also likely to be associated with the reduction in stomatal conductance and transpiration that occurs under elevated CO2 (Long et al., 2004; Ainsworth and Rogers, 2007; Wullschleger and Strahl, 2010; Wertin et al., 2010). Lower transpiration will lead to increased leaf (Morison and Gifford, 1984; Idso et al., 1987) and canopy temperatures (Lawlor and Mitchell, 1991; Kimball et al., 1995), reducing growth and biomass partitioning (White and Reynolds, 2003; Farooq et al., 2011). It is also possible that the 3 ◦ C above the ambient temperature at which the plants were grown accelerated phenology, shortening the time for carbon fixation and biomass accumulation (Rawson, 1992; Wang et al., 1992; Bowes, 1996; Dias de Oliveira et al., 2013). Measurements of nitrogen (N) uptake were not made in this study, but it is likely that the combined effect of elevated CO2 with high temperature reduced the capacity of the root system for capturing N since N uptake and root biomass and length are correlated (Liao et al., 2006). The contrasting response in total plant biomass between the non-vigorous cultivar Janz and the vigor line Vigor 18 under elevated CO2 was associated with increased leaf area, leaf and stem biomass and the production of tillers in Janz. Similar findings were recently reported for a pair of sister wheat lines contrasting in vigorous growth (Benlloch-Gonzalez et al., 2014). Because the early shoot and root growth of Vigor 18 is vigorous and responsive to water and nitrogen supply (Liao et al., 2004, 2006; Palta et al., 2007), a positive response in shoot and root growth was expected under elevated CO2 . This was not observed. However, the non-vigorous cultivar Janz increased its root biomass and total root length under elevated CO2 . In fact, elevated CO2 stimulated below-ground growth in greater proportion than above-ground biomass. Thus, the differences in total plant biomass between the two genotypes under elevated CO2 were mainly due to an increase in root biomass in the nonvigorous cultivar Janz. Comparing the below-ground response to elevated CO2 obtained in this study with those from a previous study using a pair of sister lines contrasting in vigor it appears that the vigor trait in wheat may inhibit plasticity in growth in response to elevated CO2 . This finding does not support our original hypothesis.

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Wide and thin leaves and faster development of leaf area through production of wider leaves rather than leaf and tiller number are characteristics of the vigorous trait in wheat (Rebetzke and Richards, 1999; Botwright et al., 2002). Wide and thin leaves are also characteristics that may limit the strength response of the initial sink (leaf) to an increase in photosynthetic carbon under elevated CO2 (Paul and Foyer, 2001; Ainsworth et al., 2004). Low tiller number also reduced the strength response of the sink and an adequate sink strength response to increasing photosynthetic carbon in wheat crops is essential for maximising the growth response to elevated CO2 (Aranjuelo et al., 2011). This implies that the sink strength response to an increase in photosynthetic carbon is small in genotypes with the vigor trait. Elevated CO2 increases growth in wheat by stimulating tillering (Gifford, 1977; Sionit et al., 1981), but in this study, an increase in tillering under elevated CO2 occurred in the non-vigorous cultivar Janz and not in the vigorous line Vigor 18. Since tillering was not responsive to elevated CO2 in the line Vigor 18, leaf area was not affected, mainly because increases in leaf area are associated with increases in the number of tillers. Nodal roots in wheat are an important component of the root system and their production is also associated with the tillering capacity of the genotype (Hockett, 1986; Palta and Watt, 2009). Consequently, the failure in tillering production in Vigor 18 was reflected in its root biomass and length. A similar failure in tillering production under elevated CO2 was recently reported for the highest vigorous line 38–19 (Dias de Oliveira et al., 2013). 5. Conclusions Root biomass was enhanced by elevated CO2 under both ambient and high temperature, but the positive effect of elevated CO2 was less when plants were grown under high temperature. A similar effect was observed in shoot biomass. Total root length increased under elevated CO2 only when plants were grown under ambient temperature. No effect in total root length occurred when plants were grown under high temperature. There were differences between the two genotypes in the effect of elevated CO2 in most of the above- and below-ground biometric parameters measured. Janz responded positively to elevate CO2 , but no effect was observed in the vigorous line Vigor 18. The rate of root extension was enhanced by elevated CO2 under both temperatures in Janz, but this effect was greater under ambient than under high temperature. In Vigor 18, elevated CO2 only enhanced the rate of root extension under ambient temperature, but the increase was lower than in the cultivar Janz. Acknowledgments We thank Samuel Henty for his technical assistance. Dr. María Benlloch-Gonzalez thanks the Ministerio de Educación of the Spanish Government under the National Program for the Mobility of Human Resources of Investigation I-D+i 2008–2011 and CSIRO for the support that made her visit to Western Australia possible. This research was supported by the Australian Department of Agriculture, Fisheries and Forestry (DAFF). References Acock, B., Acock, M.C., Pasternak, D., 1990. Interactions of CO2 enrichment and temperature on carbohydrate production and accumulation in muskmelon leaves. J. Am. Soc. Hortic. Sci. 115, 525–529. Ainsworth, E.A., Rogers, A., 2007. The response of photosynthesis and stomatal conductance to rising [CO2 ]: mechanisms and environmental interactions. Plant Cell Environ. 30, 258–270. Ainsworth, E.A., Rogers, A., Nelson, R., Long, S.P., 2004. Testing the “source–sink” hypothesis of down-regulation of photosynthesis in elevated [CO2 ] in the field with single gene substitutions in Glycine max. Agric. For. Meteorol. 12, 85–94.

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