Effect of soil compaction on photosynthesis and carbon partitioning within a maize–soil system
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Soil & Tillage Research 71 (2003) 151161
Effect of soil compaction on photosynthesis and carbonpartitioning within a maizesoil system
Ashraf Tubeileh a,, Virginie Groleau-Renaud b, Sylvain Plantureux b,Armand Guckert b
a Department of Soil and Irrigation, Palestinian Ministry of Agriculture, P.O. Box 1217, Nablus, Palestineb Laboratoire Agronomie et Environnement, INPL (ENSAIA)-INRA, BP 172, 54505 Vandoeuvre-ls-Nancy, France
Received 21 August 2002; received in revised form 20 January 2003; accepted 26 January 2003
Soil compaction is known to affect plant growth. However, most of the information regarding the effects of this factor oncarbon partitioning has been obtained on young plants while little is known about the evolution of these effects with plantage. The objective of this work was to investigate how soil compaction affects carbon assimilation, photosynthate partitioningand morphology of maize plants during vegetative growth up to tassel initiation. A pressure was applied on moist soil toobtain a bulk density of 1.45 g cm3 (compacted soil (CS) treatment) while the loose soil (LS) treatment (bulk density of1.30 g cm3) was obtained by gentle vibration of soil columns. Plants were grown in a growth chamber for 36 weeks andcarbon partitioning in the plantsoil system was evaluated using 14C pulse-labelling techniques. Soil compaction greatlyhampered root elongation and delayed leaf appearance rate, thereby decreasing plant height, shoot and root dry weights andleaf area. The increase in soil bulk density decreased carbon assimilation rate especially in early growth stages. The main effectof soil compaction on assimilate partitioning occurred on carbon exudation, which increased considerably to the detrimentof root carbon. Furthermore, soil microbial biomass greatly increased in CS. Two hypotheses were formulated. The first wasthat increasing soil resistance to root penetration induced a sink limitation in roots and this increased carbon release intothe soil and resulted in a root feedback that regulated carbon assimilation rate. The second hypothesis relies on soilplantwater relations since, due to compaction, the pore size distribution has to be considered. In a compacted soil, the peak of thepore size distribution curve is shifted towards the small pore size. The volume of small pores increases and the unsaturatedconductivity decreases substantially, when compared to non-compacted soil. Due to small hydraulic conductivity, the inflowinto the roots is well below optimum and the plant closes stomata thus reducing carbon assimilation rate. The effects of soilcompaction persisted with plant age although the difference between the two treatments, in terms of percentage, decreased atadvanced growth stages, especially in the case of root parameters. 2003 Elsevier Science B.V. All rights reserved.
Keywords: Carbon; Morphology; Photosynthesis; Plant age; Root exudation; Soil compaction
Corresponding author. Present address: Natural ResourcesManagement Program, International Center for Agricultural Re-search in the Dry Areas (ICARDA), P.O. Box 5466, Aleppo, Syria.Tel.: +963-21-2213477x551; fax: +963-21-2213490.E-mail address: firstname.lastname@example.org (A. Tubeileh).
Compaction is a change in soil structure that de-creases its porosity and increases its penetrationresistance. This constraint results in restricted rootgrowth that in turn may affect the whole plant growth
0167-1987/03/$ see front matter 2003 Elsevier Science B.V. All rights reserved.doi:10.1016/S0167-1987(03)00061-8
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and grain yield (Canarache et al., 1984). The mostpronounced effect of soil compaction is the reductionof root length. Several authors have observed suchan effect under different growth conditions. Logsdonet al. (1987) indicated that increasing soil bulk den-sity caused a linear decrease in maize root length withthe increase in soil bulk density. Similar results wereobtained with different crops (maize, barley, wheat,peas and beans) and various culture media (soil andnutrient solution with glass beads) (Abdalla et al.,1969; Asady and Smucker, 1989; Kayombo et al.,1991; Grath and Hkansson, 1992; Oussible et al.,1992; Groleau-Renaud et al., 1998). Meanwhile, theeffect of soil compaction on root biomass depends oncompactness degree, soil water status, and soil phys-ical properties. For instance, while Atwell (1990a)observed that soil compaction increased root biomassof wheat, other authors have shown that increasingcompactive stress decreases root dry weight of maize(Panayiotopoulos et al., 1994). These morphologi-cal modifications probably affect water and nutrientuptake.
Soil compaction effects extend beyond root mor-phology, affecting both shoot morphology and gen-eral plant physiology. A reduction in leaf area andshoot biomass was observed in maize plants grownon compacted soil (Ekwue and Stone, 1995). Further-more, several authors have reported a decrease in pho-tosynthetic activity due to a drop in stomatal con-ductance in plants grown on compacted soils (Masleet al., 1990; Tardieu et al., 1992). This decrease wasattributed to a chemical message, mainly abscisic acid(ABA), produced in the stressed roots and travelling toshoots via the xylem sap (Masle et al., 1990; Tardieu,1994).
Carbon partitioning within the maizesoil systemwas the subject of several papers (Liljeroth et al.,1994; Qian et al., 1997). However, the effect of soilcompaction on carbon partitioning has rarely been in-vestigated. Studying carbon partitioning under differ-ent bulk densities is of major interest as it determinesroot:shoot ratio and grain yield. Sauerbeck and Helal(1986) labelled maize plants continuously from day7 to day 23 in order to study photosynthate distribu-tion. They reported increases with increasing soil bulkdensity in both the fraction of carbon recovered in thesoil and in that respired by roots and soil microorgan-isms. On the other hand, 14C remaining in roots de-
creased with increasing soil strength. Similarly, rootexudation was stimulated when roots of young maizeplants were impeded in a glass bead nutrient solution(Boeuf-Tremblay et al., 1995). A main shortage in ex-isting data is that they were obtained using very youngplants (up to 3 weeks old). Moreover, some of the pre-vious works were conducted in hydroponic conditionsthat do not represent soil conditions.
The aim of the present paper is to track the evolu-tion of the effects of soil compaction on photosynthe-sis, carbon partitioning (including in the rhizosphere)and plant morphology of maize plants ageing from 21to 42 days (shortly before tassel initiation). We areparticularly interested in the effect of soil bulk densityon carbon budget in the maizesoil system and on soilmicrobial biomass.
2. Materials and methods
The culture medium used in this study was a mix-ture of sand and sandy loam soil. Soil was air-driedand sieved to pass a 5 mm mesh before being mixedwith 2 mm sieved sand (two-thirds to one-third). Themineral composition of the final mixture was 12.6%clay, 13.5% silt and 73.9% sand, while total carboncontent was 1.5%. The total porosity of the mixture(bulk density 1.3 g cm3) was around 50% whileits field capacity was 23% (w/w). The mixture wasthen packed into polyvinyl chloride (PVC) cylinders(40 cm 15.5 cm inner diameter) and the cylinderswere closed at the bottom with a mesh to ensure goodaeration of the soil column. A 2 cm gravel layer sep-arated the soil from the mesh at the bottom.
The soil mixture was moistened and uniformlypacked in the cylinders with gentle vibration to obtainthe bulk density of 1.3 g cm3, which represented theloose soil (LS). Meanwhile, the CS (bulk density of1.45 g cm3) was prepared using a soft pressure ex-erted by hand. The height of the soil layer was 35 cmand that of headspace was 3 cm.
Maize seeds (Zea mays L., cv. Dea) were germi-nated on agar for 72 h in darkness at 25 C and uni-form plantlets were selected. Thereafter, one plantletwas planted in each soil cylinder and placed in agrowth cabinet programmed to run at 16 h photope-riod, with a photosynthetic photon flux density (PPFD)of 300400mol m2 s1, and temperatures of 23 C
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by day and 18 C by night. Relative humidity wasmaintained at 6575% and soil water content was keptat 15% of soil dry weight throughout the growth pe-riod. Preliminary studies showed that this level is op-timum for maize growth under our conditions. Waterlosses were estimated and compensated by weighingevery 2 days and plants were irrigated with Hoaglandand Arnon (1938) nutrient solution. For all the ex-periments detailed below, the plants were grown un-der these conditions from the first day after planting(DAP). However, for technical reasons the plants werenot planted at the same time.
2.1. Morphology experiment
Five plants were harvested at 21, 35 and 42 DAPin soil columns. Plant height, number of visibleleaves, root number and length of main root axeswere measured at harvest. Leaf area was determinedusing Analyra 1995 software (CIRAD, Montpellier,France). This software calculates leaf area by multi-plying the number of pixels by their size. Shoot androot dry weights were determined after being dried at60 C for 3 days.
2.2. Carbon assimilation experiment
Photosynthetic activity of plants grown on com-pacted and loose soils was studied twice a week fromthe age of 21 DAP to the age of 42 DAP. This pa-rameter was measured in three plants for each dateand treatment. At each date, the rootsoil compart-ment of an individual plant was air-tightly sealed inorder to separate soil and root respiration from that ofthe ambient atmosphere (Fig. 1). The sealing was ob-tained using liquid silicone (Rhodorsil, base+catalyst,Aventis, France). An individual plant was placed in aplexiglass growth chamber with the same environmen-tal conditions mentioned previously. Measurementswere taken around noon and carbon assimilation byall plant leaves was determined by tracing the lineardecrease curve of CO2 concentration inside the cham-ber. The slope of the straight line represents CO2 up-take per minute for the whole plant. This value wasthen divided by leaf area and calculated in terms ofmol CO2 m2 s1. CO2 concentration was measuredusing a Li-6200 (Li-Cor, Lincoln, NE, USA) infraredgas analyser.
2.3. Carbon partitioning experiment
At each date, six plants, three for each treatment,were selected to be labelled with 14C at 21, 35 and42 DAP. These plants were placed in the plexiglasschamber 1 day prior to the date of experiment. Eachcylinder was placed in another PVC container andshoots were sealed at the soil surface in a way to en-sure air tightness of belowground compartments (rootsand soil) as shown in Fig. 1. After hardening of thesealant, columns were transferred to the growth cabi-net and appropriate connections for water supply andsoil aeration were set up.
14C was generated by adding sulphuric acid toNa2H14CO3. Specific activity inside the chamberwas constant (14 MBq g1 C) in all experiments butlabelling duration varied according to assimilationrate. Labelling started at a CO2 concentration of360mol mol1 and continued until a concentrationof 120mol mol1 was reached (two-thirds of carbonpresent was assimilated). Preliminary experimentsindicated that, for short periods, carbon assimilationwas constant in this range. The labelling process var-ied with plant age and lasted for 120, 26 and 19 minfor 21-, 35- and 42-day-old plants, respectively. Soilwas continuously aerated during the experiment andthe chase period in order to avoid root anoxia.
Fig. 1. A schematic diagram illustrating a cross-section of culturepot and the air-tight separation of underground compartments.
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At harvest, shoots were cut at the soil surface andleaves were separated from the stem. The soil columnwas pushed out of the cylinder and roots were care-fully excavated and gently washed in tap water to re-move adherent rhizosphere soil. Plant components andsoil-containing solution were placed immediately at25 C. They were then freeze-dried and the biomassof each compartment (shoots, roots and soil) was de-termined.
Total carbon content of each compartment was de-termined using a Carlo Erba CNS Na 1500 analyser(Carlo Erba Instrumentazione, Milan, Italy). 14C inshoots and roots was detected using a Flo-One/Beta(Packard, Meriden, CT, USA) solid scintillation anal-yser coupled with the Carlo Erba analyser. Soil ra-dioactivity was determined by burning a soil sample ina Carmograph (Wsthoff, Germany) and the resulting14CO2 was collected and counted with a Packard liq-uid scintillator (Packard Instrument, Downers Grove,IL, USA).
2.4. Soil microbial biomass
Soil microbial biomass was determined for threeplants per treatment and per date (21, 35 and 42 DAP).After removal of the remaining root fractions, the soilof each pot was homogenised and two samples werekept at 25 C. Soil moisture content at analysiswas close to 50% of field capacity. A pre-extractionwith 0.05 M K2SO4 solution was performed in orderto eliminate remaining root fractions that were notpicked up manually (Mueller et al., 1992). Micro-bial biomass was determined using the chloroformfumigationextraction method described by Vanceet al. (1987). Organic carbon content in soil extractswas determined by a DC 190 carbon analyser (DC190, Dohrmann, Germany). The following formulawas used to determine soil microbial biomass carbon:
SMBC = CorgFS CorgCSKC
where CorgFS is the organic carbon resulting from fu-migated soil, CorgCS the organic carbon resulting fromcontrol (non-fumigated) soil, and KC the conversionfactor (0.45).
Since the amount of carbon released from fumigatedsoil does not account for the total carbon of soil mi-
crobial biomass, a proportionality coefficient (KC) of0.45 was used throughout (Jenkinson and Ladd, 1981).
The experiments were performed according to acompletely randomised design. All the results wereanalysed by ANOVA using Statistica 5 (1995) soft-ware. Thereafter, means were compared by means ofLSD at the level of P < 0.05 unless otherwise indi-cated.
As expected, increasing soil bulk density decreasedsoil porosity. At 15% moisture content, air-filledporosity occupied 29% of the total volume for CStreatment versus 35% for LS treatment. However, bothaeration levels were not growth limiting according toWolkowski (1990).
3.1. Plant growth
Soil compaction greatly hampered root elongation.For 21-day-old plants (DAP), the mean lengths ofnodal and seminal root axes were 30% less in CS thanin LS (Table 1). However, between the ages of 35 and42 days mean length of seminal root axes levelled offin the LS treatment while it continued to grow in CS.Consequently, the difference between the two treat-ments decreased to slightly more than 10% at the fi-nal harvest. In the case of nodal r...