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Alignment of lipid bodies along the plasma membrane during the acquisition of desiccation tolerance in maize seed. (Seed Physiology, Production & Technology).

ORTHODOX SEED (tolerant to desiccation) in contrast to recalcitrant seed (sensitive to desiccation) undergo severe dehydration in the final stage of their life cycle. Before dehydration, these seeds accumulate specific storage compounds such as nonreducing sugars, phospholipids, and late-embryogenesis-abundant proteins, which may protect against the deleterious effects of water loss. Unlike most other cultivated crops, hybrid maize seed is usually harvested at moisture contents >400 g [H.sub.2]O [kg.sup.-1] fw and mechanically dried to about 120 g [H.sub.2]O [kg.sup.-1] fw. Thus, the dehydration phase takes place in an artificial dryer, with heated air as the energy source to remove water at higher rates than under natural environmental conditions. Seed quality is often reduced by artificial drying, although the impairment mechanisms remain poorly understood.

Although several chemical and molecular mechanisms associated with desiccation tolerance have received attention in the last decade, few studies have addressed ultrastructural changes during this event. Klein and Pollock (1968) observed that polysomes disappeared and ribosomes appeared free in cell cytoplasm of embryo axes of lima beans (Phaseolus lunatus L.) during maturation. Depletion of plastid starch during acquisition of desiccation tolerance has been reported in mustard (Sinapis alba L.) embryos (Fisher et al., 1988) and in radicle cells of Brassica campestris L. embryos (Leprince et al., 1990). This depletion of plastid starch corresponded with the appearance of stachyose and increases in sucrose (Leprince et al., 1990). Berjak et al. (1992) observed fewer vacuoles at maturity as compared with significant increases during early germination in Landophia kirkii Dyer. Farrant et al. (1997) observed that seed of Avicennia marina (Forsk.) Vierh. (a recalcitrant tropical species) remained highly vacuolated during maturation and did not accumulate insoluble reserves; on the other hand, Aesculus hippocastanum L. (a recalcitrant temperate species) and Phaseolus vulgaris L. (an orthodox species) decreased the level of vacuolation and increased the deposition of insoluble reserves. Moreover, mitochondria and endomembranes degenerated during the development of A. hippocastanum and P. vulgaris seed, but remained unchanged in A. marina seed. Perdomo and Burris (1998) reported that lipid bodies, first observed scattered throughout the cell cytoplasm in radicle meristem of maize seed, migrated toward the plasma membrane during preconditioning drying in seed harvested at 400 and 500 g [H.sub.2]O [kg.sup.-1] fw. Peterson (1997) observed that lipid body migration toward plasma membrane was impaired in maize seed harvested at MC > 400 g [H.sub.2]O [kg.sup.-1] fw and subjected to fast drying conditions. The ultrastructural event of lipid body alignment along the plasma membrane leads to further speculation as to their potential function as well as to mechanism(s) for alignment. The present study was conducted to investigate further the movement of lipid bodies toward the plasma membrane and their potential to regulate water loss from embryo tissue and acquisition of desiccation tolerance. Preconditioning drying treatments followed by fast drying (fluidized bed) were used as a desiccation hardiness model. Lipid bodies were detected by transmission electron microscopy and acquisition of desiccation tolerance was quantified by electrical conductivity of seed leakage and several other seed quality tests.

MATERIAL AND METHODS

Plant Material

Ears of the hybrid [B73 x sister line (H99 x H95)] were harvested in 1998, 1999, and 2000 at about 550, 500, 400, and 320 g [H.sub.2]O [kg.sup.-1] fw. At each harvest, ears at similar maturation stages were subjected to preconditioning (PC) [ear drying, at 35[degrees]C air temperature, 0.47 m [s.sup.-1] air flow rate, and about 25% relative humidity (RH)] for 0, 12, 24, 36, and 48 h. After PC, the ear-mid portion was hand shelled and subjected to fluidized bed or fast drying (35[degrees]C air temperature, 5.10 m [s.sup.-1] airflow rate, and about 25% RH) and dried down to about 130 g [H.sub.2]O [kg.sup.-1] fw. Additionally, as negative controls, ears were dried the entire period at PC (35[degrees]C) and unheated air (NH) conditions. For all the treatments, three replications of five ears were used. The experimental layout by harvest was a randomized complete block design considering dryers as blocks.

Alignment of Lipid Bodies

Transmission electron microscope (TEM) observations were made before fast drying of the embryo axes of seed harvested in 2000 at 500 g [H.sub.2]O [kg.sup.-1] fw preconditioned for 0, 24, 48, and 72 h. Additionally, axes of seed harvested at 400 and 320 g [H.sub.2]O [kg.sup.-1] fw with 0 h PC were observed for the effect of maturation on the alignment of lipid bodies. Axes were prepared according to the protocol used by Perdomo and Burris (1998) with the following modifications: (i) no staining with aqueous uranyl acetate; (ii) dihydration times were double for fresh seed. In brief, five axes were immediately excised and place in fixative solution consisting of 20 g [kg.sup.-1] paraformaldehyde, 20 g [kg.sup.-1] glutaraldehyde, 1.0 mM calcium chloride, and 0.05 M phosphate buffer, pH 7.2, for 24 h at 4[degrees]C. Axes were then rinsed and placed in fixative solution containing 10 g [kg.sup.-1] osmium tetroxide in 0.05 M phosphate buffer for 24 h at 4[degrees]C. Then, axes were dehydrated in ethanol series of 25, 50, 70, 95, and 100 g [kg.sup.-1]. Axes were imbibed with Spurr's resin (standard mixture of the Spurr's Kit)/acetone series and finally cast with pure resin. Cross sections of about 80 nm of the radicle meristem (Fig. 1A) were examined and photographed in root cap (1), outer quiescent center (QC) cells (2), and inner QC cells (3) (Fig. 1B) with a JEOL 1200EX STEM (Peabody, MA) and Kodak SO-163 film. To assess the effect of fast drying rates on the alignment of lipid bodies, embryo axes of seed having been dried under the different drying treatments in 1998 were processed for TEM as described above but photographs were only taken in the inner QC cells of the radicle.

[FIGURE 1 OMITTED]

Alignment of LB and Acquisition of Desiccation Tolerance

Alignment of lipid bodies is related to embryo drying rates and seed quality data (Cordova-Tellez and Burris, 2002). In brief, drying rates were calculated from measurements of moisture content (MC) of three replications of five intact seeds and five excised embryos. Standard germination test (SGT) was conducted in rolled towel (7 d at 25[degrees]C) in four replications of 25 seeds per treatment. Seedlings classified as normal in SGT according to Association of Official Seed Analysts Rules (1992) were separated into shoot and root and dried at 105[degrees]C for 24 h to obtained shoot to root ratio. These values are reported as an additional variable in this publication. Electrical conductivity was measured using the Individual Seed Analyzer, Genesis-2000, in four replication of 25 seeds per treatment. Dry matter accumulations of intact seed and excised embryo were measured in three replications of 10 intact seeds and 10 embryos by the oven method (105[degrees]C, 24 h).

Trends in MC and seed quality were analyzed by harvest in all three years. Since trends were similar in all three years, we present data obtained in 2000 for MC and data obtained in 1998 for seed quality parameters. We only present some figures, and the reader is referred to Cordova-Tellez and Burris (2002, this issue) for more details. Visualization of lipid bodies depends upon microscopy technique and cell cutting location (Fig. 1C, D). Thus, to illustrate the alignment of lipid bodies along the plasma membrane we will refer to cells with visualization of the nucleus, which may indicate that the cutting occurred at or closer to the central section of the cell.

RESULTS

Alignment of Lipid Bodies

In seed harvested at 500 g [H.sub.2]O [kg.sup.-1] fw (about 530 g [H.sub.2]O [kg.sup.-1] fw embryo MC), LB were dispersed throughout the cytoplasm in root cap, outer QC cells, and inner QC cells (Fig. 2A, B, C). After 24 h PC, LB were aligned along the plasma membrane in root cap and partially aligned in outer QC cells, but they remained scattered throughout the cytoplasm in inner QC cells (Fig. 2D, E, F). As preconditioning progressed, LB began aligning in inner tissues. After 48 h PC (500 g [H.sub.2]O [kg.sup.-1] fw embryo MC, Fig. 3A), they were completely aligned in the outer QC cells and in the alignment process in the inner QC cells (Fig. 2G, H). Then, following 72 h PC (400 g [H.sub.2]O [kg.sup.-1] fw embryo MC, Fig. 3A), LB alignment in the inner QC cells was completed (Fig. 2I).

[FIGURES 2-3 OMITTED]

Under field drying, alignment of LB followed a trend similar to PC drying, that is, from the periphery (root cap) toward inner QC cells. In seed harvested at 400 g [H.sub.2]O [kg.sup.-1] fw (500 g [H.sub.2]O [kg.sup.-1] fw embryo MC), LB were in the alignment process (some are aligned) in root cap cells (not shown) and outer QC cells (Fig. 2J), but they were scattered throughout the cytoplasm of the inner QC cells (not shown). In seed harvested at 320 g [H.sub.2]O [kg.sup.-1] fw (440 g [H.sub.2]O [kg.sup.-1] fw embryo MC), LB were completely aligned in root cap cells (not shown) and outer QC cells and in the alignment process in the inner QC cells (Fig. 2K, L).

The fast drying rates of the fluidized bed severely disturbed the alignment of LB. Cell plasmolysis and aberrations of or coalescence of LB were evident in seed harvested at MC >400 g [H.sub.2]O [kg.sup.-1] fw and dried in the fluidized bed without PC (Fig. 4A). The severity of these aberrations was less in embryo axes of seed harvested at 400 g [H.sub.2]O [kg.sup.-1] fw than 500 and 550 g [H.sub.2]O [kg.sup.-1] fw harvests (Fig. 4A, B). These cell aberrations were not evident in seed harvested at 320 g [H.sub.2]O [kg.sup.-1] fw and fast dried without PC (Fig. 4C). Preconditioning before fast drying also exhibited a positive effect on the alignment of LB. Radicle meristem cells of seed harvested at 550 and 500 g [H.sub.2]O [kg.sup.-1] fw that had been preconditioned for 48 h before rapid drying showed some round LB aligned along the plasma membrane (Fig. 4D, E). Although atypically shaped LB were observed in these treatments, they were also aligned along the plasma membrane. Ultrastructural improvements such as alignment of LB, shape of LB, observation of nucleus and nucleolus were more evident in seed harvested at 500 than at 550 g [H.sub.2]O [kg.sup.-1] fw, both with 48 h PC. Alignment of LB and normal cell morphology was observed in seed harvested at 550 and 500 g [H.sub.2]O [kg.sup.-1] fw and dried entirely at PC (Fig. 4F) and unheated-air (NH, micrograph not shown) treatments. The impaired alignment of LB observed under the FB conditions (fast drying rates) suggests the importance of slow or moderate embryo drying rates to achieve well-organized alignment of LB along the plasma membrane.

[FIGURE 4 OMITTED]

Alignment of LB and Acquisition of Desiccation Tolerance

Embryo water content decreased rapidly down to about 420 g [H.sub.2]O [kg.sup.-1] fw in seed harvested at MC > 500 g [H.sub.2]O [kg.sup.-1] fw (Fig. 3B) and subjected to fast drying without PC. This coincided with failure in alignment of LB before fast drying. About 420 g [H.sub.2]O [kg.sup.-1] fw embryo MC appears to be a breaking point for slight decreases in embryo drying rates, which appears to coincide with alignment of LB along the plasma membrane all across the embryo radicle cells. Alignment of LB occurred from root cap cells toward the inner core cells either with PC or field drying. This coincided with slight deceases in embryo drying rates, concomitant with steadier trends in embryo water loss (Fig. 3C) under fluidized bed drying. This suggests that alignment of LB along the plasma membrane may change water relations within the cell, concomitant with a decrease in area exposed to water loss around the cell periphery.

Cell aberrations, particularly in the LB, observed in seed harvested at MC >500 g [H.sub.2]O [kg.sup.-1] fw and fast dried without preconditioning coincided with very high cell solute leakage as quantified by electrical conductivity and 0% germination in SGT (SGT) (Fig. 5A, B). As harvest was delayed (400 g [H.sub.2]O [kg.sup.-1] fw, 0 h PC), LB aberrations decreased in severity with concomitant decreases in cell solute leakage and enhanced germination. Those conductivity and germination values, however, were not comparable to those obtained from seed dried the entire period at the PC (35C) and NH treatments. Seed harvested at 320 g [H.sub.2]O [kg.sup.-1] fw and fast dried without PC, on the other hand, exhibited the lowest cell solute leakage and 100% germination; values that were similar to those observed in seed dried entirely at PC and NH treatments. These results coincided with the lowest disturbances in the alignment of LB along the plasma membrane after the fast drying conditions. Decreases in cell solute leakage and enhanced germination with PC treatments (Fig. 5A, B) are also associated with better alignment of LB and only minor aberrations. Very low cell solute leakage and high germination percentages were obtained even in seed harvested at MC > 500 g [H.sub.2]O [kg.sup.-1] fw as long as they were dried entirely at the PC and NH treatments. These treatments also achieved complete alignment of LB.

[FIGURE 5 OMITTED]

Shoot-to-root ratio was very high in seed harvested at 400 g [H.sub.2]O [kg.sup.-1] fw with 0 h PC and in seed harvested at 500 g [H.sub.2]O [kg.sup.-1] fw with 24 h PC before fast drying (Fig. 5C). With advancing maturation (320 g [H.sub.2]O [kg.sup.-1] fw) and preconditioning treatments, shoot-to-root ratio decreased to values closer to those obtained from seed dried entirely at the PC and NH treatments. Most seedlings obtained in early PC treatments in seed harvested at 550 g [H.sub.2]O [kg.sup.-1] fw were vigorous, suggesting that those seeds may have "escaped" the drying effect perhaps because of advanced maturation. This may result in the trend of shoot-to-root ratio observed at this harvest. Changes in this quality variable are also associated with better alignment of LB.

DISCUSSION

The LB in seed harvested at moisture contents > 500 g [H.sub.2]O [kg.sup.-1] fw were scattered throughout the cell cytoplasm across the radicle tissues. Both PC drying and field maturation promoted the migration of LB toward the plasma membrane. Alignment occurred first in root cap cells followed by outer and inner QC cells. This migration pattern suggests that cell water loss might be associated with the movement of LB toward the cell wall, although we do not discard the participation of other unidentified processes. Water from the embryo axes is probably removed from the outer most radicle tissues first during drying and, as drying progresses, water from internal tissues may move through intercellular domains toward the periphery to diminish a gradient created by drying (Plate 4A-D). Thus, we speculate that as water leaves the cells, lipid bodies may move with it until they reach the plasma membrane. Although embryo moisture decreased only slightly (from 530 to 500 g [H.sub.2]O [kg.sup.-1] fw) during PC in seed harvested at 500 g [H.sub.2]O [kg.sup.-1] fw (Fig. 3A), this water loss may be sufficient to trigger the alignment of LB in root cap and outer QC cells from where water may have been removed. Longer drying at the PC conditions, however, may be required to remove water from the inner QC cells and consequently alignment of LB along the plasma membranes, which appears to occur above 400 g [H.sub.2]O [kg.sup.-1] fw embryo MC (Fig. 3A; Fig. 2I). These observations are in agreement with the finding of Perdomo and Burris (1998) who reported that LB were more aligned along the plasma membranes in radicle meristem cells of maize seed harvested at MC > 400 g [H.sub.2]O [kg.sup.-1] fw under PC drying conditions that allowed removal of seed moisture. LB were partially aligned in root cap and outer QC cells in seed harvested at 400 g [H.sub.2]O [kg.sup.-1] fw (about 500 g [H.sub.2]O [kg.sup.-1] fw embryo MC) but were completely aligned in those cells in seed harvested at 500 g [H.sub.2]O [kg.sup.-1] fw (500 g [H.sub.2]O [kg.sup.-1] fw embryo MC) with 48 h PC. This difference in alignment of LB in embryos with equal MC may be associated with accumulation of storage compounds that substitute for water space and maintain cell turgor pressure in seed harvested at 400 g [H.sub.2]O [kg.sup.-1] fw. This hypothesis is supported by the linear increase in accumulation of dry matter in intact seed and embryo from 550 to 400 g [H.sub.2]O [kg.sup.-1] fw (Fig. 6). Fisher et al. (1988) reported that embryo axes of mustard seed were able to retain turgor pressure during desiccation despite severe intact seed water loss. From 400 to 320 g [H.sub.2]O [kg.sup.-1] fw harvests there is a remarkable decrease in the rate of dry matter accumulation for both intact seed and embryo (Fig. 6). Dehydration during this period may occur through intercellular domains as illustrated in Fig. 2 (Cordova-Tellez and Burris, 2002). Consequently, this may be associated with the alignment of LB in root cap and outer QC cells, and partial alignment in inner QC cells in seed harvested at 320 g [H.sub.2]O [kg.sup.-1] fw (430 g [H.sub.2]O [kg.sup.-1] fw embryo MC).

[FIGURE 6 OMITTED]

Peterson (1997) reported impairment in the alignment of LB along the plasma membrane in ears harvested at MC > 400 g [H.sub.2]O [kg.sup.-1] fw and dried in a fluidized bed drier. Under the drying treatments used in this study, we observed not only impairment in the alignment process because of the fast drying rates exhibited in the fluidized bed, but also cell plasmolysis and aberrations of or coalescence of LB. LB aberrations appear to be more severe in those seeds subjected to fluidized bed drying before alignment of LB along the plasma membrane. These aberrations decreased in severity with both PC and field maturation, conditions that promote the movement of lipid bodies toward the plasma membrane. In addition, our observations support the finding of Peterson (1997) that seed harvested at early maturation stages (in our case >500 g [H.sub.2]O [kg.sup.-1] fw) are able to achieve alignment of lipid bodies as long as they are dried slowly. This in turn revealed the importance of slow embryo drying rates down to about 400 g [H.sub.2]O [kg.sup.-1] fw (below 300 g [H.sub.2]O [kg.sup.-1] fw intact seed MC), which appears to be the point at which LB are aligned across all radicle meristem cells. This is not suggested as a general recommendation because we evaluated only one genotype. This threshold level may vary, and needs to be investigated further.

The occurrence of aberrations or perhaps coalescence of LB remains unexplained, although it may be associated with the formation of the lipid body itself. Lipid or oil bodies are composed of a matrix of triacylglycerols, surrounded by a phospholipid monolayer, and a set of interfacial proteins termed "oleosins" (Huang, 1992; Murphy, 1993). Huang (1992) and Cummins et al. (1993) proposed that one of the physiological roles of oleosins is to prevent coalescence of oil bodies as they come close to one another during maturation drying. However, there is controversy in the literature on how and when oleosins become part of the lipid body surface. Cummins et al. (1993) found that dehydration of oil bodies from young embryos of Brassica napus L. resulted in the breakdown and coalescence into large clumps that could not be reemulsified, even after rehydration. In contrast, the oleosin-rich oil bodies from mature embryos were stable to dehydration and subsequent rehydration. Although oleosin and triacylglycerols accumulation occurred at overlapping periods in seed of B. napus, Coriandrum sativum L., and Hordeum vulgare L., the maximal rate of net triacylglycerols accumulation considerably preceded that of oleosin (Aalen, 1995; Murphy and Cummins, 1989; Ross and Murphy, 1992). Concomitant oleosin and oil accumulation from 13 to 33 d after planting has been reported for maize embryos (Tzen et al., 1993). Nevertheless, we used different hybrid and harvesting was started about 33 d after planting. Additionally, we do not discard the possibility that cell plasmolysis may restrict cell area on such a large scale that cutting through the middle of the cell becomes difficult (Fig. 1D). In such restricted space, lipids may bind to each other and in the one-dimensional sections we observe clusters or aberrations. Thus, further research is required to clarify the disturbance observed in the alignment of LB along the plasma membrane.

LB alignment along the plasma membrane appears to be involved in regulating cell water loss from embryo tissues. The rapid decline in embryo MC to about 420 g [H.sub.2]O [kg.sup.-1] fw in early harvests (550 and 500 g [H.sub.2]O [kg.sup.-1] fw) under rapid drying occurred before alignment of LB. As alignment of LB along the plasma membrane is taking place either with PC or field maturations, embryo-drying rates appear to slightly decrease and subsequently water loss occurs in a more organized fashion. These observations suggest that alignment of LB along the plasma membrane may decrease cell surface exposed to loss of water, which may lead to a change in water relations within the cells and consequently more organized dehydration during seed drying.

Perdomo and Burris (1998) and Peterson (1997) reported that alignment of LB along the plasma membrane was associated with low cell solute leakage and enhanced germination, and our results are in agreement. Additionally, we observed higher performance in cold test, "soak test" (germination after conductivity test), and seedling dry weight (data not shown) and lower shoot-to-root ratios in those treatments that exhibited better alignment of LB. Accelerated aging test percentages were above 60% germination only with embryo MC about 400 g [H.sub.2]O [kg.sup.-1] fw before fast drying and alignment of LB across the radicle meristem cells (data not shown). This result suggests impairment in other mechanisms, variation in seed maturation, or both. In general, alignment of LB along the plasma membrane may regulate embryo-drying rate and contribute in the acquisition of desiccation tolerance as expressed by lower cell solute leakage and high germination performance under diverse germination conditions. Alignment of LB appears to be a common phenomenon and has been reported during seed maturation in embryos of P. vulgaris (Dasgupta et al., 1982), B. campestris (Leprince et al., 1990), Cuscuta pedicellata Ledeb. and C. campestris Yuncker (Lyshed, 1992), and white spruce [Picea glauca (Moench) Voss] somatic embryos (Misra et al., 1993). Farrant et al. (1997) presented micrographs of embryos of recalcitrant and orthodox species. Alignment of LB is evident in dry radicle meristem of P. vulgaris but not in the recalcitrant species Avicennia marina and Aesculus hipocastanum at their developmental stage 3. Nevertheless, none of these authors refer to LB alignment mechanism and participation on desiccation tolerance.

We conclude that the alignment of LB is a progressive process that occurs from the periphery of the radicle to the inner core cells in the embryo. Slow cell water withdrawal may participate in the movement of LB toward the plasma membrane. Alignment of LB along the plasma membrane may change water relations in the cell, leading to a more organized dehydration during seed drying. Rapid embryo drying rates may impair alignment of LB along the plasma membrane and are associated with low seed quality.

Abbreviations: LB, lipid bodies; PC, preconditioning; NH, unheated-air; MC, moisture content; QC, quiescent center; RH, relative humidity; fw, fresh weight.

ACKNOWLEDGMENTS

The authors wish to thank Independent Professional Seedsmen Association and Pioneer Hi-bred International for funding this study. The authors would also like to thank the Bessey Microscopy Facility at Iowa State University and Tracy Pepper for taking the micrographs. The senior author is grateful to Consejo Nacional de Ciencia y Tecnologia (CONACYT) and Colegio de Postgraduados for the funding provided for his Ph.D. studies.

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Leobigildo Cordova-Tellez and Joseph S. Burris *

L. Cordova-Tellez, Colegio de Postgraduados (IREGEP), Montecillo Edo. de Mexico, 56230, Mexico; J.S. Burris, Burris Consulting, 1707 Burnett Ave., Ames, IA 50010. Journal Paper No. J-19439 of the Iowa Agriculture and Home Economics Exp. Stn., Ames, IA 50011. Project No. 3603. Received 31 July 2001. * Corresponding author (burrisconsulting@msn.com).
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Date:Nov 1, 2002
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