<<

HortTechnology October – December 1998 8(4)

Understanding Systems to Improve, Quality

Silvana Nicola 1

SUMMARY. Root architecture can be very important in productivity. The importance of studies on root morphology and development is discussed to improve seedling growth. Root systems of dicotyledonous species are reviewed, with emphasis on differences between growth of basal and lateral . The presence of different types of roots in plant species suggests possible differences in function as well. The architecture of a root system related to its functions is considered. Classical methods for studying root systems comprise excavation of root system, direct observation, and indirect analyses. While the first method is destructive and the third is effective in understanding root architecture only on a relatively gross scale, observation methods allow the scientist a complete a nondestructive architectural study of a root system. The three groups are reviewed related to their potential to give valuable information related to the root architecture and development of the seedling, with emphasis on the availability of a medium-transparent plant-growing system, enabling nondestructive daily observations and plant measurements under controlled environmental conditions. Effects of CO2 enrichment on seedling growth is reviewed, emphasizing the effects of CO2 on root growth.

Vigorous root systems are as essential as vigorous for growth and development of healthy . Early seedling root growth and development determine the optimum root system throughout the entire life of a plant, consequently affecting growth during this period and potentially leading to optimization of yields (Leskovar and Stoffella, 1995; Lynch, 1995). The spatial distribution in the of the root system can determine the potential of a plant to exploit the soil's resources, which are unevenly distributed on Earth's surface or subjected to localized depletion by the roots (Lynch, 1995). The production of a primary root system, i.e., the primary branching from the , may have a major impact on growth and survival of a plant (MacIsaac et al., 1989). A primary root system increases the surface area available for the uptake of and mineral elements. In addition, with its architecture, a primary root system provides physical support to the developing .

Morphology and development of young roots in dicotyledonous species

Seedling root morphology differs between monocotyledonous and dicotyledonous species (Fahn, 1982; Leskovar and Stoffella, 1995; Sutton and Tinus, 1983; Zobel, 1975, 1986, 1995, 1996). Dicotyledonous species were described as presenting three types of roots: radicle, adventitious, and lateral (Esau, 1965, 1977).

The radicle forms the (pri- and upper portion of the al., 1979), and lettuce (Lactuca sativa mary root), adventitious roots are taproot. Assuming only three types of L.) (Nicola, 1997). initiated from the hypocotyl, and root, the double homozygote should Evidence that basal and lateral roots lateral roots are from the taproot. have had only a taproot. Because these differ in terms of morphology, point of Beginning with Zobel (1975), several roots were genetically not lateral, nor origin from the taproot and researchers have identified a fourth were they adventitious, Zobel (1975) development was reported by Nicola type of roots-basal roots. Zobel (1986) classified these roots as basal roots. (1997) in lettuce grown in indicated that initiation of basal roots is Basal roots have been reported to be transparent medium (Fig. 1). Basal and under different genetic control than produced by mungbean (Vigna radiata lateral roots in lettuce seedlings initiation of lateral and adventitious L.) (Leskovar and Stoffella, 1995), bell originated from two distinct re gions of roots. In fact, a double homozygote pepper (Capsicum annuum L.) the taproot and developed differently. from a lateralless tomato mutant (Leskovar et al., 1989; Stoffella et al., A thicker, short upper radicle was (recessive mu tant called diageotropica, 1988), tomato (Lycopersicon esculen- visibly distinguished from a smaller, dgt) and an adventitiousless tomato tum Mill.) (Zobel, 1975), beans long, lower radicle 2 d after seeding mutant (recessive mutant called (Phaseolus vulgaris L.) (Stoffella et (DAS). This distinction was even more , ro ) originated roots in the evident 3 and 4 DAS. A restriction area

1 Dipartimento di Agronomia, Selvicoltura e Gestione del Territorio,Universita di Torino, Via Leonardo da Vinci, 44, 10095 Grugliasco (TO), Italy; e-mail: [email protected]. HortTechnology October – December 1998 8(4) separated the two portions of the defined lateral roots as "roots derived hypothesized that basal roots would taproot. Basal roots originated at two from lateral endogenous primordia provide a means for plants to uptake opposite sides of the short upper formed in preexisting roots" (p. 149). surface-applied and water portion of the taproot and located close The author said that lateral roots during crop production, and they may to the hypocotyl, and did not produce appeared at a relatively constant also play a role in supporting the plant secondary during the first 18 distance behind the tip of a growing (Bole, 1977; Eshel and Waisel, 1996; DAS. Lateral roots originated at ˜120o root, that lateral roots initiated in rows Jackson, 1995). Findings in lettuce that apart along the longer portion of the or ranks, and that within each rank they lateral roots originated in three taproot and produced secondary appeared to initiate and emerge in directions with respect to the taproot, branches. Basal roots presented a acropetal sequence under normal at 120o apart and extending deep in the horizontal extension in the medium, conditions. Charlton (1996) reported soil, is an indication that lateral roots while lateral roots presented a growth that between the basipetally emerged can explore more soil volume for extension downward into the medium. lateral roots, particularly in dicots, resources than basal roots, thus lateral The number of lateral roots 18 DAS additional latera ls may arise for a long roots may be able to reach and exploit was 2- to 3-fold the number of basal period in roots with . localized patches of nutrients in the roots. Esau (1965) referred to these soil (Lynch, 1995). Conversely, basal Adventitious roots cannot be con- additional lateral roots as adventitious. root bidirectional and superficial founded with lateral roots for two main formation gives the root system a reasons. First, adventitious roots The architecture of a root horizontal extension in the soil surface, originate from the stem, while lateral system related to its function assuring the basal roots the capacity to roots originate from the taproot. exploit the most fertile portions of Second, the former type originates Fitter and Stickland (1991) and agricultural (Bole, 1977; Eshel from tissues other than the , Lynch and van Beem (1993) suggested and Waisel, 1996). while the latter type originates from the that the architecture of a root system Zobel (1996) reported that species pericycle. Conversely, basal roots are may have ecological implications for that demonstrated the most drought not clearly classified with respect to uptake of water and nutrients from soil. tolerance had the most deeply penetrat- their point of initiation. Zobel (1986) Fitter (1986, 1987, 1996) suggested ing root system, implying that plants demonstrated that basal roots initiate that, in general, plants with a more with an extensive system from the pericycle of the lower herringbone-like distribution of roots, would be favored in these instances. hypocotyl and upper taproot. Con- that is, with branches mainly along the Eshel and Waisel (1996) suggested that sequently, basal roots were not central root axis, may occur under low the major function of basal roots was adventitious in anatomical origin, nor soil resource availability, whereas in to exploit the most fertile portions of lateral or adventitious in genetic plants with a dichotomous-like distri- agricultural soils more efficiently than control of their initiation (see above). bution, secondary branches increase lateral roots. In addition, Bole (1977) Detailed information of the when resources are present in abundant found that basal roots of rape (Brassica sequence of events occurring in root supply, thereby increasing acquisition campestris L.) were capable of forma tion of young seedlings of water and nutrients. Variation in absorbing more efficiently could be valuable to further determine root architecture among species was the root development of field-grown indicated by Seiler (1994) to be an plants. In bell pepper seedlings, basal important factor determining differ- roots emerged prior to lateral roots ences in among (Stoffella et al., 1988) and only after species. Early, rapid root growth and full expansion. A similar branching were suggested to confer an development was found in lettuce adaptive advantage in more efficient seedlings (Nicola, 1997). In tomato use of soil water. Root elongation can seedlings, lateral roots emerged before be advantageous to plants in drying basal roots (Aung, 1982). Weinhold soil, and may be particularly important (1967) described basal roots as arising for seedling establishment. Growth of acropetally (toward the shoot apex) new plants is restricted largely to from the germinating seedling, while surface soil layers that are vulnerable lateral roots arose basipetally (toward to drying (Sharp et al., 1988). the radicle apex). Nicola (1997) Basal roots differ from the three reported in lettuce a similar devel- more classic types in terms of opment only for the first 8 to 10 DAS, morphology, , and thereafter basal and lateral roots development (Nicola, 1997; Zobel, emerged also between older primary 1996). This suggests possible differ- Fig. 1. Diagram of lettuce seedlings 18 d branches, contemporary to emergence ences in function as well. The differen- after seeding. The different types of roots of basal and lateral roots that followed tiated functions of basal and lateral present in lettuce seedlings are shown: taproot, basal and lateral roots, and lateral the respectively original acropetal and roots have not yet been fully secondary branches basipetal patterns. Charlton (1996) understood, but several authors have HortTechnology October – December 1998 8(4) than lateral roots. Eshel and Waisel same volume of soil and root system to supply of growth substances as does an (1996) reported that basal roots were be observed continuously. The major explant or a and they can grow less sensitive to gravity than lateral constraint in using these methods is autotrophically if provided sufficient roots, and therefore could extend the that only a portion of the root can be CO2. When using airtight vessels for root system horizontally. observed, and extrapolation of the root growing photoautotrophic seedlings,

measurements to the entire root system the CO2 concentration was often mea- Studying seedling root systems may be not representative. If a whole sured to be as low as the CO2 comp en- root viewing surface could be devel- sation point (less than 100 µmol?mol-1) Studies on root morphology and oped, observation methods could rep- during most of the photoperiod architecture have attracted much re- resent a major advance for study of the (Fujiwara et al., 1987; Kozai et al., search in the field of and root system. Although hydroponic liq- 1992). Using loose caps or gas perme- crops, since these species have a long uid culture allows direct observation of able film for capping the growth life span and have a high dependence the entire root system, present growing vessels resulted in CO2 concentrations on water supply, fertility, soil physical conditions prevent normal often <200 µmol?mol-1 (Kozai, 1991) property, and aeration. As early as development. (which is lower than the atmospheric 1927, Weaver and Bruner (1927) The extent and activity of the root concentration of 350 µmol?mol-1). lamented the lack of studies on how a system have been indirectly measured During the dark period, CO2 root system functions. During the by relating the root function to supply concentration to 3000 to 9000 1980s interest in studying roots of water and mineral nutrients to the µmol?mol-1, but remained low (100 to increased, particularly related to the plant (Mackie-Dawson and Atkinson, 200 µmol?mol-1) for the entire light regulation of root growth and develop- 1991), For example, a relationship be- period. ment (Feldman, 1984). tween root length and maximum soil IN VITRO METHOD. Little Measurements of root and moisture depletion was observed in research has been conducted in vitro root length are typically used to de- pasture species by Evans (1978). using and even fewer studies scribe root distribution in the soil pro- Consequently, variation in soil have been done using in vitro culture file, but analysis of root morphology moisture with depth as determined by to study root architecture and and architecture can improve the un- measurement of soil water potential morphology. Stoffella et al. (1988) derstanding of water and ex- has been used for estimating root used test tubes filled with gelled traction from soil (Fitter, 1985). How- activity through mathematical models. medium (gelrite) supplemented with 32 ever, field methods to study root devel- Similarly, the absorption of P was mineral nutrients and sucrose as a car- opment with repeated direct observa- found to be correlated with root length bon source (photomixotrophic growth), tions of undisrupted root growth have by Atkinson (1989). This relationship to characterize the early root morphol- been extremely limited (Mackie- was studied using a combination of an ogy of bell pepper seedlings. A whole- Dawson and Atkinson, 1991). observation window in a laboratory plant observation method was imple- CLASSICAL METHODS. Meth- study and the injection of the mented to study the early root growth ods to study the root system and radioisotope in the soil. These indirect and development of lettuce seedlings reviewed by Mackie-Dawson and methods can be effective in under- (Nicola, 1997; Nicola et al., 1996). Atkinson (1991) include 1) excavation standing root architecture, however, Nicola et al. (1996) and Nicola (1997) of the root system, 2) direct only on a relatively gross scale used test tubes filled with Phytagel observation, and 3) indirect analyses. (Mackie-Dawson and Atkinson, 1991). gelled medium supplied with mineral Methods from the first group require MICROPROPAGATION ME- nutrients and sucrose to grow lettuce the removal of the root system from THOD. Another approach to the study seedlings and study root morphology the soil, usually by washing, and can of early seedling root growth is that of and architecture [photomixotrophic cause a major loss of root material micropropagation in culture, whole plant culture (PMWPC)]. Plants when dealing with young seedlings. particularly where all external carbon were grown 9 d in the tubes and then Early in development, much of the root is derived from CO2 (Kozai, 1991). In removed. The lack of recyclable air system is very fragile, making full this type of autotrophic culture, growth and depth for root extension did not excavation and architectural analysis and development are largely influenced permit further growth. Consequently, a extremely difficult (Jackson, 1995). In by physical environmental factors photosynthetic whole-plant culture studying root systems actively growing which include light, CO2, humidity, air (PWPC) system was designed and built in soil, Jackson (1995) felt that a major flow speed, temperature, and O2. by Nicola (1997) to study seedling root difficulty was the extraction of fine However, use of photoautotrophic growth, which attempted to remove the roots and the measurement of root micropropagation of whole seedlings is exogenous sucrose supply as a carbon architectural variables. fairly new, and considerations should source and introduce circulating fresh Observation methods require a be taken as, e.g., how the physical air into the plant container to avoid the viewing surface that is inserted into the environment affects photoautotrophic lowering of CO2 concentrations during soil (Mackie-Dawson and Atkinson, growth and development of whole the light period. Glass 1-L bottles were 1991). The development of the root seedlings. used to accommodate a large quantity system in situ can then be seen through Seedlings originated from seeds of transparent nutrient medium, thus a window into the soil, allowing the and grown in vitro do not require a permitting the growth of seedlings for HortTechnology October – December 1998 8(4) up to 18 DAS without supplying 50% increase in . altered root mo rphology and archi- sucrose as a carbon source. Filtered The increase in atmospheric CO2 tecture are also related to water and and calibrated air was allowed to flow increases photosynthetic efficiency in nutrient acquisition capacity from soil in and out the bottles, thus permitting terrestrial C3 plants because the present of the root system (Fitter, 1985; Fitter the seedlings to use their photo- CO2 concentration is insufficient to and Stickland, 1991; Lynch and van synthetic capacity. Environmental saturate the ribulose-1,5-bisphosphate Beem, 1993). Using CO2 enrichment in conditions of the growth room such as carboxylase/oxygenase enzyme system a controlled environment would be a temperature, relative humidity and (Rubisco) and the increased CO2 valuable approach to increase early light were preconditioned and competitively inhibits ribulose-1,5-bis - root branching in seedlings during controlled throughout the duration of phosphatc oxygenation and photores- greenhouse transplant production. the experiments. The growing system piration (Long et al., 1996). However, developed was easily constructed, an acclimation effect occurs, and the Conclusions calibrated and monitored during lettuce rate of photosynthesis again declines in seedling root growth studies, and many species, mainly due to a decline Root growth, development and ar- enabled direct nondestructive plant ob- of rubisco activity (Evans, 1983,1987; chitecture are important aspects of servations and measurements, under Geiger and Servaites, 1991; Kramer, seedling growth. Stresses reduce root controlled environmental conditions. 1981; Sage et al., 1989; Sonnewald et growth, root volume and extent of root During the studies a pregerminated al., 1996; Torisky and Servaites, 1984). soil exploration. If root growth was transferred one into each Tremblay et al. (1987) increased declines due to stress, the supply of bottle and grown until plant harvest. growth rates of shoot and roots of water and nutrients to the shoot may be Number of lateral and basal roots, celery transplants raised in green- reduced, with a subsequent reduction -1 number of secondary root branches and houses with 1000 µmol?mol CO2, in shoot growth. However, conditions of could be counted daily by compared to ambient CO2 concen- that limit photosynthesis can reduce visual observation through the bottle. tration. Lettuce yield in a tunnel was shoot growth, limit assimilate trans- The root growth observation method enhanced by enrichment of CO2 in the location to the roots, and in turn, can developed could represent a valuable air (Enoch et al., 1970; Wittwer and limit root growth. There fore, stress tool to investigate root morphology Robb, 1964). Del Castillo et al. (1989) originating in either the root or shoot and development in different species, found that (Glycine max [L.] affects whole plant growth (Brown and to improve selection and breed new Merril) plants grown in growth Scott, 1984; Miller, 1986). varieties based on root architectural chambers under elevated CO2 Studies relating the effects of the characteristics. concentration had greater root mass environment immediately after radicle than those grown under normal protrusion can provide valuable Increasing root growth with atmospheric CO2 concentration. How- insights into implications of root CO2 ever, CO2 concentration did not affect perturbation on early seedling growth the rate of elongation of individual and subsequent . Increased concentration of CO2 in the roots. The number of branches Understanding root architecture is atmosphere has received more interest increased because of CO2 enrichment, important to improve transplant quality in recent years (Eshel and Waisel, resulting in an increased total root and production. Lack of methods to 1996). Plant adaptation to rising CO2 length, without an increase of the study root growth, which enable direct concentrations in the atmosphere is a volume of soil explored by the roots. observation of the roots without their paramount priority presently, because Aguirrezabal et al. (1993) studied root disruption, generally limits the study of it is estimated that CO2 in the systems in hydroponically grown sun- root architecture. A medium-trans- atmosphere will double from the 1978 (Helianthus annuus L.) as parent whole-plant method for average concentration of 338 affected by carbon . The studying early root growth is available -1 µmol?mol by the middle or later part results they obtained indicated that the and might be used for precise and st of the 21 century (Murray, 1995). control of carbon partitioning among accurate nondestructive plant measure- Enrichment of atmospheric CO2 has various components of a single root ments under controlled environmental been reported to increase growth rate svstem was determined by a conditions. It could be a valuable tool and yield of a wide variety of plant combination of the distance of each to investigate root morphology and species, and it is used in greenhouse sink from the source and its level of development in different species, to crop production in northern latitudes branching. Studies of Nicola (1997) on better study, select and breed new for cucumber (Cucumis sativus L.), to- lettuce seedlings grown in a controlled varieties based on root architectural mato, celery (Apium gravoeolens L.), environment have indicated that potential. Although architectural and lettuce (Calvert, 1972; Calvert and enriching the atmosphere up to 2000 changes of root systems caused by -1 Slack, 1975; Challa, 1976; Gent, 1984; µmol?mol CO2 enhanced root branch environmental conditions may occur Knight and Mitchell, 1988; Tremblay formation in the seedlings, particularly without noticeable biomass changes in et al., 1987; Wittwer and Robb, 1964). basal roots, compared to the control of the whole seedling, they might affect -1 Sonnewald et al. (1996) reported that 350 µmol?mol C02, without affecting the transplant stand establishment and the initial response to elevated CO2 in plant biomass 18 DAS. The ecological subsequent yield of vegetable crops. the atmosphere could lead to about a and physiological implications of such

HortTechnology October – December 1998 8(4)

systems. II. Influence of nutrient sup- Esau, K. 1977. Anatomy of seed ply on architecture in contrasting plant nd Literature cited plants. 2 ed. Wiley, New York. species. New Phytol. 118:383-389.

Aguirrezabal, L.A.N., S. Pellerin, and Eshell A., and Y. Waisel. 1996. Fujiwara, K., T. Kozai, and I. F. Tardieu. 1993. Carbon nutrition, Multiform and multifunction of various root branching and elongation: Can the Watanabe. 1987. Measurements of constituents of one root system, p. present state of knowledge allow a carbon dioxide gas concentration in 175-192. In: Y. Waisel, A. Eshel, and closed vessels containing tissue predictive approach at whole-plant U. Kafkafi (eds.). Plant roots: The level? Environ. Expt. Bot. 33:121-130. cultured plantlets and estimates of net hidden half. Marcel Dekker, Inc., New photosynthetic rates of the plantlets. J. Atkinson, D. 1989. Root growth and York. Agr. Met. 43:21-30. activity: current performance and Evans, JR. 1983. Nitrogen and photo- future potential. Aspects Appl. Biol. Geiger, D. R. and J.C. Servaites. 1991. synthesis in the flag leaf of Carbon allocation and responses to 22:1-13. (Triticum aestivum L.). Plant Physiol. stress, p. 103-127. In: H.A. Mooney, 72:297-302. Aung, L.H. 1982. Root initiation in W.E. Winner, and E.J. Pell (eds.). tomato seedlings. J. Amer. Soc. Hort. Response of plants to multiple stresses. Evans, JR. 1987. The relationship Academic Press, San Diego, Calif. Sci. 107:1015-1018. between electron transport components

Bole, J.B. 1977. Uptake of tritiated and photosynthetic capacity in Gent, M.P.N. 1984. Carbohydrate level water and phosphorus-32 by roots of leaves grown at different irradiances. and growth of tomato plants. I. The Austral. J. Plant Physiol. 14:157-170. wheat and rape. Plant Soil 46:297-307. effect of carbon dioxide enrichment

and diurnally fluctuating temperatures. Calvert, A. 1972. Effects of day and Evans, P.S. 1978. Plant root Plant Physiol. 76:694-699. night temperatures and carbon dioxide distribution and water use patterns of enrichment on yield of glasshouse some pasture and crop species. N.Z. J. Jackson, L.E. 1995. Root architecture tomatoes. J. Hort. Sci. 47:231-247. Agr. Res. 21:261-265. in cultivated and wild lettuce (Lactuca

rd spp). Plant Environ. 18:885-894. Calvert, A., and G. Slack. 1975. Fahn, A. 1982. . 3 ed. Effects of carbon dioxide enrichment Pergamon Press, New York. p. Knight, S.R. and C.A. Mitchell. 1988. 253-287. on growth, development and yield of Effects of CO2 and photosynthetic photon flux on yield, gas exchange and glasshouse tomatoes. I. Responses to Feldman, L.J. 1984. Regulation of root controlled concentrations. J. Hort. Sci. growth rate of Lactuca sativa L. development. Annu. Rev. Plant 'Waldmann's Green'. J. Expt. Bot. 50:61-71. Physiol. 35:223-242. 39:317-328.

Challa, C. 1976. Analysis of the Fitter, A.H. 1985. Functional signifi- Kozai, T. 1991. Photoautotrophic diurnal course of growth, carbon cance of root morphology and root micropopagation. In vitro Cell. Dev. dioxide exchange, and carbohydrate system architecture, p. 87-106. In: reserve content of cucumber. Agr. Res. Biol. 27:47-51. A.H. Fitter (ed.). Ecological inter- Rpt. Wageningen 861. actions in soil. Blackwell Scientific Kozai, T., K. Fujiwara, M. Hayashi, Charlton, W.A. 1996. Lateral root Publications, Oxford, U.K. and J. Aitken-Christie. 1992. The in initia tion, p. 149-173. In: Y. Waisel, A. vitro environment and its control in Fitter, A.H. 1986. The topology and micropopagation, p. 247-282. In: K. Eshel, and U. Kafkafi (eds.). Plant geometry of plant root system roots: The hidden half. Marcel Dekker, Kuraka and T. Kozai (eds.). Transplant architecture: Influ ence of watering rate production systems. KluwerAca- Inc., New York. on root system topology in Trifolium demic Publishers, Dordrecht, The Del Castillo, D., B. Acock, V.R. pratense. Ann. Bot. 58:91-101. Netherlands.

Reddy, and M.C. Acock. 1989. Elon- Fitter, A.H. 1987. An architectural gation and branching of roots on Kramer, P.J. 1981. Carbon dioxide approach to the comparative ecology soybean plants in a carbon dioxide concentration, photosynthesis, and dry of plant root system. New Phytol. 106 matter accumulation. Bioscience -enriched aerial environment. Agron. J. (Suppl.):61-77. 81:692-695. 31:29-33.

Leskovar, D.I., D.J. Cantliffe, and P.J. Enoch, H., I. Rylski, and Y. Samish. Fitter, A.H. 1996. Characteristics and Stoffella. 1989. Pepper (Capsicum function of root system, p. 1-20. In: Y. 1970. CO2 enrichment to cucumber, annum L.) root growth and its relation lettuce and sweet pepper plants grown Waisel, A. Eshel, and U. Kafkafi to shoot growth in response to in low plastic tunnels in a subtropical (eds.). Plant roots: The hidden half. nitrogen. J. Hort. Sci. 64:711-716. climate. Israel J. Agr. 20:63-69. Marcel Dekker, Inc., New York.

Leskovar, D.I. and P.J. Stoffella. 1995. Esau, K. 1965. Plant anatomy. 2nd ed. Fitter, A.H., and T. R. Stickland. 1991. Vegetable seedling root systems: Wiley, New York. Architectural analysis of plant root HortTechnology October – December 1998 8(4)

Morphology, development, and impor- Nicola, S., D.J. Cantliffe, and K.E. Torisky, R.S. and J.C. Servaites. 1984. tance. HortScience 30:1153-1159. Koch. 1996. Sucrose enhances initia- Effect of irradiance during growth of tion of lateral and basal roots in lettuce. Glycine maxon photosynthetic capacity Long, S.P., B.G. Drake, P.K. Farage, 10th FESPP Congr. "From molecular and percent activation of ribulose M. Frehner, R.L. Garcia, G.R. Mechanisms to the Plant: An Inte- 1,5-bisphosphate carboxylase. Photo- Hendrey, S.R. Humphries, P.J.jr. grated Approach". 9-13 Sept. 1996, synth. Res. 5:251-261. Pinter, B.A. Kimball, G.W. Wall, G.Y. Firenze, Italy. Plant Physiol. Bio chem. Nie, and C.P. Osborne. 1996. Spec. Issue. p. 50-51. Tremblay, N., S. Yelle, and A. Acclimation of photosynthesis to el- Gosselin. 1987. Effects of CO2 enrich- evated C02 and the interaction with Sage, R.F., J.D. Sharkey, and J.R. ment, nitrogen and phosphorus nitrogen in big "pots". Proc. 2nd Intl. Seemann. 1989. Acclimation of photo- fertilization on growth and yield of IGBPGCTE Workshop "Plant Acclim- synthesis to elevated CO2 in five C3 celery transplants. HortScience ation to elevated CO2", 19-23 May, species. Plant Physiol. 89:590-596. 22:875-876. 1996, Lake Tahoe, Calif. p. 38-41. Seiler, G.J. 1994. Primary and lateral Weaver, J.E. and W.E. Bruner. 1927. Lynch, J. 1995. Root architecture and root elongation of sunflower seedlings. Root development of vegetable crops. plant productivity. Plant Physiol. Environ. Expt. Bot. 34:409-448. McGraw Hill, New York. p. 320-3333. 109:7-13. Sharp, R.E., W.K. Silk, and T. Hsiao. Weinhold, L. 1967. Histogenetische Lynch, J. and J.J. van Beem. 1993. 1988. Growth of the primary studien zum grenzwurzel-problem. Growth and architecture of seedling root at low water potentials. Plant Beitr. Biol. Pflanzen. 43:367-454. roots of common bean genotypes. Crop Physiol. 87:50-57. Sci. 33:1253-1257. Wittwer, S., and W. Robb. 1964. Sonnewald, U., K.P. Krause, F. Carbon dioxide enrichment of MacIsaac, S.A., V.K. Sawhney, and Y. Ludewig, R. Zrenner, and K. Herbers. greenhouse atmo sphere for food crop Pohorecky. 1989. Regulation of lateral 1996. Transgenic plants to study plant production. Econ. Bot. 18:34-56. root formation in lettuce (Lactuca responses to elevated atmospheric CO2 sativa) seedling roots: Interacting concentrations. Proc. 2nd Intl. Zobel, R.W. 1975. The genetics of root effects of anaphthalenacetic acid and IGBP-GCTE Workshop "Plant Accli- development, p. 261-275. In: J.G. kinetin. Physiol. Plant. 77:287-293. mation to elevated CO2", 19-23 May Torry and D.F. Clarkson (eds.). The 1996, Lake Tahoe, Calif. p. 12-15. development and function of roots. Mackie-Dawson, L.A. and D. Academic, London. Atkinson. 1991. Methodology for the Stoffella, P.J., M. Lipucci Di Paola, A. study of roots in fie ld experiments and Pardossi, and F. Tognoni. 1988. Root Zobel, R.W. 1986. Rhizogenetics (root the interpretation of results, p. 25-47. morphology and development of bell genetics) of vegetable crops. Hort- In: D. Atkinson (ed.). Plant root peppers. HortScience 23:1074-1077. Science 21:956-959. growth: An ecological perspective. Zobel, R.W. 1995. Genetic and Blackwell, Boston. Stoffella, P.J., R.F. Sandsted, R.W. Zobel, and W.L. Hymes. 1979. Root environmental aspects of roots and Murray, D.R. 1995. Plant responses to characteris tics of some black beans: II. seedlings stress. HortScience carbon dioxide. Amer. J. Bot. Morphological differences among 30:1189-1192. 82:690-697. genotypes. Crop Sci. 19:823-830. Nicola, S. 1997. Lettuce (Lactuca Zobel, R.W. 1996. Genetic control of root systems, p. 21-30. In: Y. Waisel, sativa L.) root morphology, architec- Sutton, R.F. and R.W. Tinus. 1983. ture, growth and development in an Root and root system terminology. A. Eshel, and U. Kafkafi (eds.). Plant autotrophic culture system. PhD diss. Monogr. 24. For. Sci. (suppl.) roots: The hidden half. Marcel Dekker, Inc., New York. Univ. Florida, Gainesville. 29:1-137.