Free-Air [CO.sub.2] Enrichment Effects on Apex Dimensional Growth of Spring Wheat.
Environmental factors also affect apex size in wheat. Friend (1965) found that increasing temperature from 10 to 30 [degrees] C enhanced the rate of apex elongation. Holmes (1973) reported that shorter photoperiods produced a longer inflorescence apex at equivalent stages, while Griffiths and Lyndon (1985) observed that vernalization led to a shorter apex at equivalent stages. The effect of nitrogen on apex growth remains unclear. For example, Frank and Bauer (1982) showed that varying nitrogen levels had no effects on apex size, whereas Longnecker et al. (1993) revealed that nitrogen deficiency slowed the rate of primordia initiation.
In the only known study of [CO.sub.2] concentration on apex growth of wheat, Frank and Bauer (1996) found a significant increase in apex length and width with a 950 [micro] mol [mol.sup.-1] [CO.sub.2] enrichment at temperature between 22 and 26 [degrees] C although a significant interaction existed between temperature and [CO.sub.2] concentration. Several researchers have noticed an increase in the rate of primordium initiation beginning with initiation of the spikelet primordia (Friend, 1965; Kirby, 1977; Baker and Gallagher, 1983; Li et al., 1997), but so far no systematic observations are available on how apical dome dimensional growth relates to the increase in rate of primordium initiation. The information on apex growth is very limited compared with the amount of research on apex primordium initiation. We found no literature on the rates of elongation and widening of the apex dome under elevated [CO.sub.2] concentrations, or on the relationship between the rates of primordium initiation and the size of inflorescence apices.
The present investigation was initiated to quantify the dimensional growth of the wheat apex and to determine the response of the apex to elevated [CO.sub.2] environments for different culms. In a previous study, Li et al. (1997) reported that elevated [CO.sub.2] significantly increased the number of floret primordia of T2, T3, T10, and T11 tillers, but not the number of spikelet primordia. We will relate apex dimensional growth and spikelet or floret primordium numbers in this paper to further the understanding of the physiological bases of yield potential formation under elevated [CO.sub.2] concentrations.
MATERIAL AND METHODS
Sampling and Dissecting
Spring wheat (`Yecora Roja') was grown at elevated (550 [micro] mol [mol.sup.-1]) or ambient (370 [micro] mol [mol.sup.-1]) [CO.sub.2] concentrations with four replications in the Free-air [CO.sub.2] Enrichment System (FACE) located on the demonstration farm at the University of Arizona Maricopa Agricultural Center. The experimental design and growth conditions were previously described by Li et al. (1997). Sampling commenced on 2 Jan. 1993, 4 d after 50% of the plants had emerged. Samples were collected at 3- to 4-d intervals until the end of floret primordium initiation. Seven to 11 plants were randomly sampled from each plot, and three of these were subsampled and dissected to the apex. After dissections, apex lengths and widths were measured on fresh material with a stage micrometer. During initiation of the vegetative primordia, apex length was measured as the distance from the base of the last initiated leaf primordium to the tip of the apex dome. During initiation of the reproductive primordia, apex length was measured as the distance from the collar, which is a reduced leaf-like structure at the lowermost node of the spike, to the tip of the apex. Widths were always measured on the widest section of the apices (Fig. 1).
[Figure 1 ILLUSTRATION OMITTED]
Air temperatures were measured at 2 m above the soil surface, and accumulated thermal units were calculated using the equation below:
 ATU = [Sigma] ([T.sub.max] + [T.sub.min])/2 - [T.sub.b]],
where [T.sub.max] and [T.sub.min] represent daily maximum and minimum air temperatures based on hourly readings, and [T.sub.b] is the base temperature for wheat (0 [degrees] C, Bauer et al., 1985). Apex data were found to follow an exponential model given by the following:
 [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]
where A is the length or width (mm), respectively, of apices; [[Beta].sub.0] is the intercept for apex length or width curves; k is a constant for apex length or width curves and is positively related to the rate of apex elongation or widening; and x is accumulated thermal units in [degrees] C d. This model was fitted by regression on the following linearized form:
 [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]
where A* = log(A) and [MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII] = log([[Beta].sub.0]). The definitions for k and x are as above. Contrasts for parameter k between [CO.sub.2] levels was conducted with a dummy variable procedure in SAS 6.12 (SAS Institute, 1989). The [R.sup.2] values for these relationships were all greater than 0.74 for the MS and primary tillers. Only T10 and T11 among the secondary tillers had sufficient data to fit the exponential models described above, with their [R.sup.2] values ranging from 0.49 to 0.92. Missing tillers were treated as missing data.
RESULTS AND DISCUSSION
Apex Size Development
Elevated [CO.sub.2] increased the apex lengths of T2, T3, and T10 at the double ridge stage. At the terminal spikelet stage, only T3 and T10 apex lengths of elevated [CO.sub.2] grown plants were longer than those of ambient [CO.sub.2] grown plants (Table 1). In a parallel study, Li et al. (1997) did not observe a significant increase in spikelet primordia in these culms with the longer apex. At the double ridge stage, elevated [CO.sub.2] increased the apex width of T2 only, but no significant difference in apex width was detected at the terminal spikelet stage between the two [CO.sub.2] levels. At the flag leaf appearance stage, which is considered to be the completion of floret primordium initiation (Baker and Gallagher, 1983), elevated [CO.sub.2] increased the widths of T2, T3, T10, and T11 apices by 18 to 43% and increased the number of floret primordia of T2, T3, and T10 by 20 to 46% as previously observed by Li et al. (1997). The data indicate that elevated [CO.sub.2] stimulates the apex growth in length and width of later-formed tillers over ,various stages. The apices of different culms responded independently to elevated [CO.sub.2] and the general trend was that the later the tillers were formed, the more responsive the apices were to elevated [CO.sub.2].
Table 1. Inflorescence apex lengths and widths at double ridge (DR), terminal spikelet (TS), and flag leaf appearance (FLA) stages for the main stem (MS), primary tillers (T0, T1, T2, and T3), and secondary tillers (T10 and T11) at elevated (E) and ambient (A) [CO.sub.2] treatments.
Apex lengths Culms Treatments DR TS mm MS A 1.11 2.99 E 1.20 3.25 change % +8.1 +8.7 T0 A 0.90 2.84 E 1.03 3.11 change % +14.4 +9.5 T1 A 0.91 3.9 E 0.98 4.07 change % +7.7 +4.4 T2 A 1.04 3.03 E 1.22 3.35 change % +17.3 +10.6 T3 A 0.77 3.03 E 0.98 4.01 change % +27.3(*) +32.3(**) T10 A 0.75 2.86 E 0.93 4.09 change % +24.0(*) +43.0(*) T11 A 0.95 2.13 E 1.09 2.46 change % +14.7 +15.5 Apex widths Culms DR TS FLA mm MS 0.46 1.22 2.03 0.48 1.33 2.19 +4.3 +9.0 +7.9 T0 0.36 1.19 1.65 0.43 1.35 1.83 +19.4 +13.4 +10.9 T1 0.36 1.41 1.84 0.41 1.45 2.05 +13.9 +2.8 +11.4 T2 0.31 1.13 2.17 0.42 1.22 2.56 +35.5(**) +8.0 +18.0(*) T3 0.36 1.13 1.2 0.39 1.35 1.48 +8.3 +19.5 +23.3(*) T10 0.28 0.48 0.51 0.32 0.56 0.67 +14.3 +16.7 +31.4(*) T11 0.31 0.58 0.60 0.38 0.64 0.86 +22.6 +10.3 +43.3(**)
(*), (**) Significant at 0.05, 0.01 level, respectively.
Growth Dynamics of MS and Tiller Apices
The MS apex lengths of elevated and ambient [CO.sub.2] grown plants were regressed against accumulated thermal units with Eq.  (Fig. 2). The length of the MS apex increased very slowly during vegetative primordium initiation (0-126 [degrees] C d). At 180 [degrees] C d, as the apex started to change from the vegetative to the reproductive stage, apex elongation slowly increased at both [CO.sub.2] levels. The change in apex elongation per [degrees] C d was linear between 180 to 473 [degrees] C d for ambient [CO.sub.2] level and between 180 to 437 [degrees] C d for elevated [CO.sub.2] treatment during the period of spikelet primordium initiation (Li et al., 1997). In the process of floret primordia initiation, which occurs between 372 to 664 [degrees] C d for ambient [CO.sub.2] and 376 to 633 [degrees] C d for elevated [CO.sub.2] concentrations (Li et al., 1997), the apex elongated exponentially. Although the effects of elevated [CO.sub.2] on rate of apex elongation of the MS were always positive, there was no significant difference between the two [CO.sub.2] levels in apex length of the MS at the double ridge and terminal spikelet stages. These observations are in agreement with previous research in which the change in apex length correlates with early developmental stages (Holmes, 1973; Car-Smith et al., 1989). However, Car-Smith et al. (1989) reported a divergence in growth during the floret primordium initiation stage. We detected a different elongation dynamic of the MS apices between the two [CO.sub.2] levels, which was probably due to the stimulated rate of apex elongation under elevated [CO.sub.2].
[Figure 2 ILLUSTRATION OMITTED]
The apex lengths of the coleoptile tiller (T0), primary tillers (T1, T2, and T3), and secondary tillers (T10 and T11) were fitted to Eq.  (Table 2). Elongation of the tiller apices followed a pattern similar to that of the MS, (i.e., apex elongation was more linear during the earlier reproductive stage and more exponential during the later reproductive growth stage). The ranking of the equations by decreasing intercepts ([[Beta].sub.0]) was the same for either treatment and reflects the order of tiller appearance (data not shown): MS [is greater than] T1 [is greater than] T0 [is greater than] T2 [is greater than] T10 [is greater than] T3 [is greater than] T11 (Table 2). This result implies that intercepts of apex developmental curves could be used as an indicator of tiller appearance order, although the practical utilization of this finding is limited.
Table 2. Parameters for exponential regression equations of apex lengths of the main stem (MS) and tillers for ambient (A) and elevated (E) [CO.sub.2] conditions. [R.sup.2] is the coefficient of determination. The F values for testing the differences between models relating to the elevated and ambient [CO.sub.2] concentrations were generated with a dummy variable procedure in SAS. [[Beta].sub.0] and k are parameters for Eq. .
Culms Treatments [[Beta].sub.0] k [R.sup.2] F MS A 0.2099 0.0054 0.9541 3.22(*) E 0.1929 0.0061 0.9478 T0 A 0.1377 0.0053 0.7468 0.58 E 0.1361 0.0057 0.8303 T1 A 0.1490 0.0059 0.9292 2.59 E 0.1369 0.0064 0.9530 T2 A 0.1054 0.0064 0.9353 0.73 E 0.1090 0.0066 0.9585 T3 A 0.0780 0.0059 0.8016 4.55(*) E 0.0621 0.0070 0.9237 T10 A 0.0786 0.0058 0.7421 2.30 E 0.0709 0.0066 0.9250 T11 A 0.0779 0.0050 0.7289 14.86(**) E 0.0475 0.0068 0.8648
(*),(**) Significant at 0.05, 0.01 levels, respectively.
The coefficient (k) of the Eq.  was positively related to the relative elongation rate of the apex (Table 2). The ranking of the coefficients (k) for the equations reflected the decreased rates of apex elongation of later-formed tillers in plants grown at ambient [CO.sub.2] concentration (T2 [is greater than] T1 = T3 [is greater than] T10 [is greater than] MS [is greater than] T0 [is greater than] T11), and the increased rates of apex elongation of later-formed tillers in plants grown at elevated [CO.sub.2] concentration (T3 [is greater than] T11 [is greater than] T2 = T10 [is greater than] TI [is greater than] MS [is greater than] T0) (Table 2).
Figure 3 compares the apex growths of the coleoptile, primary tillers and the first secondary tiller (T11). Elevated [CO.sub.2] increased the rates of T0, T1, and T2 apex elongation by 0.0004 log(mm) [degrees] [C.sup.-1] [d.sup.-1], 0.0005 log(mm) [degrees] [C.sup.-1] [d.sup.-1], and 0.0002 log(mm) [degrees] [C.sup.-1] [d.sup.-1] respectively, and significantly increased the rate of T3 and T11 apex elongation by 0.0011 log(mm) [degrees] [C.sup.-1] [d.sup.-1] and 0.0018 log(mm) [degrees] [C.sup.-1] [d.sup.-1] (Table 2). These results indicate that the T3 and T11 apices elongated more slowly under ambient [CO.sub.2] than did those under elevated [CO.sub.2] (Fig. 3).
[Figure 3 ILLUSTRATION OMITTED]
The F-tests of the regression curves show significant differences in the dynamics of apical growth between the two [CO.sub.2] levels for T3 and T11, but not for T0, T1, T2, and T10 (Table 2). We conclude that elevated [CO.sub.2] changes the pattern of apex elongation within a plant by enhancing the apex elongation of later-formed tillers. This implies that the apex growth of later-formed tillers is more responsive to elevated [CO.sub.2] than that of earlier-formed tillers. The increased lengths, however, were not accompanied by an increase in numbers of spikelet primordia. Li et al. (1997) previously showed that numbers of spikelet primordia did not increase in MS and tillers at the same elevated [CO.sub.2] concentration in a parallel study.
Widening of Apex in the MS and Tillers
Equation  was used to regress width of the MS apex against the accumulated thermal units for ambient and elevated [CO.sub.2] concentrations (Fig. 4). The change in width of the MS apex appears to be similar in pattern to the change in apex length. The width of the apex increased slowly during the vegetative primordium initiation stage. Beginning at the double ridge stage (180 [degrees] C d) and during the spikelet primordium initiation stage, apex width increased linearly, then increased exponentially during the floral primordium initiation stage. Elevated [CO.sub.2] had a positive effect on the widening rate of the MS apex over all developmental stages. Furthermore, a difference in the pattern of MS apex widening was detected between plants grown at elevated and ambient [CO.sub.2] concentrations (Table 3).
[Figure 4 ILLUSTRATION OMITTED]
Table 3. Parameters for exponential regression equations of apex widths of the main stem (MS) and tillers for ambient (A) and elevated (E) [CO.sub.2] conditions. [R.sup.2] is the coefficient of determination. The F values for testing the differences between models relating to the elevated and ambient [CO.sub.2] concentrations were generated with a dummy variable procedure in SAS. [[Beta].sub.0] and k are parameters for Eq. .
Culms Treatments [[Beta].sub.0] k [R.sup.2] F MS A 0.2126 0.0033 0.8949 3.67(*) E 0.2092 0.0036 0.9228 T0 A 0.1374 0.0034 0.7581 1.26 E 0.1248 0.0038 0.7857 T1 A 0.1506 0.0037 0.9127 3.19 E 0.1469 0.0040 0.9330 T2 A 0.1204 0.0038 0.8608 1.66 E 0.1166 0.0041 0.8981 T3 A 0.1113 0.0032 0.8678 9.20(**) E 0.0741 0.0044 0.8847 T10 A 0.1113 0.0032 0.6278 1.02 E 0.0741 0.0044 0.8847 T11 A 0.1041 0.0028 0.4907 5.39(*) E 0.0287 0.0044 0.6603
(*),(**) Significant at 0.05, 0.01 levels, respectively.
The apex widths of the coleoptile tiller (T0), primary tillers (T1, T2, and T3) and secondary tillers (T10 and T11) were fitted to Eq.  (Table 3). The ranking of the apex width coefficients (k) was T2 [is greater than] T1 [is greater than] T0 [is greater than] T3 under ambient [CO.sub.2] and T3 [is greater than] T2 [is greater than] T1 [is greater than] T0 under elevated [CO.sub.2]. Comparison of the elevated [CO.sub.2] effects on the apex widening of the primary tillers and the first secondary tiller (T11), shows that elevated [CO.sub.2] slightly increased the rates of apex widening of T1, but greatly increased the rate of T3 and T11 apex widening (Fig. 5). Because of the fast growth rate of T3 in elevated [CO.sub.2], the completion of floret initiation was nearly synchronized with that of the earlier-formed tillers (Li et al., 1997). The width of the T11 apex at the flag leaf appearance stage in ambient [CO.sub.2] grown plants was about 0.5 mm, which reflected the abortion of T11 at this stage, while the width in elevated [CO.sub.2] reached 1.0 mm. Even though this was smaller than those of the TI, it suggests that some of the T11 apices in elevated [CO.sub.2] grown plants may have survived to develop into a spike.
[Figure 5 ILLUSTRATION OMITTED]
We detected differences in the apex widening patterns of T3 and T11 between ambient and elevated [CO.sub.2] conditions, but not for T0, T1, T2, and T10 (Table 3). Just as for apex elongation, the apex widening of later-formed tillers was more responsive to elevated [CO.sub.2] than were earlier-formed tillers.
We propose that growth of the apex should be divided into four phases based on the changes in size and shape. During the first phase, when leaf primordia are initiated, the size of apex dome changes very little. During the second phase, when passing through the single ridge stage and entering the double ridge stage, the shoot apex elongates more rapidly. During the third phase, when spikelet primordia are initiated, the apex elongates linearly because of the addition of spikelet primordia. During the fourth phase, beginning from the completion of terminal spikelet initiation, apex length increases exponentially because of rachis extension. For the MS and earlier-formed tillers, apex elongation was closely related to their developmental stages. We did not detect an increase in apex length with relatively faster elongation rates under elevated [CO.sub.2] compared with ambient [CO.sub.2]. These results agree with previous research of Holmes (1973). However, apex lengths of the later-formed tillers, T2, T3 and T10, were increased by elevated [CO.sub.2] at both the double ridge and terminal spikelet stages. This was probably due to the ample supply of carbohydrates under elevated [CO.sub.2] concentration (Smart et al., 1994). Friend (1965) believes that larger mature spikes are produced from a longer apex at the double ridge stage.
The increase in apex width reflects floret primordium initiation during the last phase of apex development. Initiation of a greater number of floret primordia may lead to an increase in grain number in the mature spike. Larger apex size, though, might contribute to the increased yield under elevated [CO.sub.2] reported in a parallel study by Pinter et al. (1996).
We still lack a consistent physiological theory for apex elongation and widening. Smith (1965) and Kirby (1971) suggest that gibberellin (GA) plays a role in meristem growth of wheat and barley. Holmes (1973) suggests that the relative rate of GA utilization rather than GA level influences meristem growth. Some recent research (Ross et al., 1992) suggests that the GA/IAA ratio might be critical to stem elongation in pea. We speculate that carbohydrate supply could be another factor which might affect apex elongation. Whether GA directs carbohydrate allocation or whether assimilate supply has feedback effects on GA levels is not clear.
In conclusion, our research indicates that elevated [CO.sub.2] affected wheat apex development, with apices of later formed tillers responding more to elevated [CO.sub.2] than those of earlier-formed tillers.
Abbreviations: FACE, Free Air [CO.sub.2] Enrichment; MS, main stem; T0, coleoptile tiller; T00, T01, T02, T10, T11, and T12, secondary tillers; T1, T2, and T3, primary tillers; GA, gibberellin.
We acknowledge suggestions for statistical analysis from Mr. William J. Price. This research was supported by Grant IBN-9652614 from the NSF/DOE/NASA/USDA Joint Program on Terrestrial Ecology and Global Change (TECO II) to the Agricultural Research Service, U.S. Dep. of Agriculture, U.S. Water Conservation Lab., Phoenix, AZ (G.W. Wall, PI), and by Grant DE-FG03-95ER-62072 from the Office of Biological and Environmental Research (OBER), Environmental Sciences Division, Dep. of Energy, Terrestrial Carbon Processing Research Program (TCP) to the Univ. of Arizona, Tucson and Maricopa, AZ (S.W. Leavitt, PI). Operational support was also provided by the Agricultural Research Service, U.S. Dep. of Agriculture, U.S. Water Conservation Laboratory, Phoenix, AZ. The FACE apparatus was furnished by Brookhaven National Laboratory, Uptown, NY, and we also acknowledge the helpful cooperation of the staff at the University of Arizona, Maricopa Agricultural Research Center, Maricopa, AZ. This work contributes to the Global Change Terrestrial Ecosystem (GCTE) Core Research Programme, which is part of the International Geosphere-Biosphere Programme (IGBP).
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Aiguo Li,(*) Gerard W. Wall, Anthony Trent, and Yuesheng Hou
A.G. Li, Dep. of Plant, Soil and Entomological Sciences, Univ. of Idaho, Moscow, ID 83844-2339; G.W. Wall, Water Conservation Lab., USDA-ARS, 4331 E. Broadway Rd., Phoenix, AZ 85040; A. Trent, Deceased, Plant Sciences, Univ. of Idaho; Y.S. Hou, Weed Science Lab., USDA-ARS, Washington State Univ., Pullman, WA 99164. Idaho Agric. Exp. Stn. Res. Paper No. 98715. Dep. of Plant, Soil and Entomological Sciences, Univ. of Idaho, Moscow, ID 83844-2339. This work was submitted by Aiguo Li in partial fulfillment of the M.S. degree. Received 10 July 1998. (*)Corresponding author (li921@ uidaho.edu).
Published in Crop Sci. 39:1083-1088 (1999).
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|Author:||Li, Aiguo; Wall, Gerard W.; Clarke, Rebecca (English composer); Hou, Yuesheng|
|Date:||Jul 1, 1999|
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