Journal of Experimental Botany, Vol. 51, No. 347, pp. 1067-1075,
June 2000
© 2000 Oxford University Press
The influence of secondary senescence processes within the culm of a pseudoviviparous grass (Poa alpina var. vivipara L.) on the supply of water to propagules
1 Department of Biological Sciences, University of Durham, South Road, Durham DH1 3LE, UK
2 Institute of Terrestrial Ecology, Bangor Research Station, Orton Building, Deiniol Road, Bangor, Gwynedd LL57 2UP, UK
Received 8 December 1999; Accepted 4 February 2000
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Abstract |
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An anatomical investigation of the culm of pseudoviviparous alpine meadow grass (Poa alpina var. vivipara L.) revealed that transpiration flow, as delimited by Lucifer Yellow tracer dye, was maintained despite advanced senescence (as evidenced by loss of chlorophyll and chloroplasts), with leafy spikelets driving transpiration flow. Transpiration flow was not hindered by cavitation or tylosis in older culms, the low frequencies of these senescence processes being bypassed via nodal plexi. Despite this, water content of plantlets declined over time and water stress became apparent, suggesting that water supply via the determinate culm was not sufficient for the increasing transpirational demand of indeterminate plantlets. The implications of declining water content on the biomechanical properties of the culm, and concomitant limitations on the pseudoviviparous reproductive strategy, are discussed. Nomenclature of grass follows Hubbard.
Key words: Poa alpina, senescence, tylosis, pseudovivipary, water.
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The propagules of grasses are connected to the parent plant both physically and physiologically via the culm, relying on this organ for both water and inorganic nutrition. The initial development of the grass culm has been described in some detail (Arber, 1934
; Gram, 1961). However, little attention has been given to the physiological events within this organ during later stages of development, and to the impact that these events may have on the development of propagules. Water loss and drying have long been assumed to be secondary senescence processes (i.e. peripheral to genetic control) apparent in the grass culm.
Aside from the biochemical consequences of water loss, drying may also have far-reaching implications for the long-distance transport of water in vascular tissues. Occlusion of the xylem vessels may result from tylosis (strictly speaking, the in-growth of companion cells through the pit membranes of the vessel walls, although occlusions may also result from the separate or associated secretion of pectic polysaccharide gels into the vessel; Rioux et al., 1998). As tylosis is either a response to net water loss from vascular tissues (Canny, 1997) or to embolism (Chattaway, 1949; Elmahjoub et al., 1984; Cochard and Tyree, 1990; Saitoh et al., 1992), and living cells may protect against embolism by excluding air (Kramer and Boyer, 1995), cavitation events and concurrent tylosis could potentially occur with age and stymie xylem transport during the development of the grass culm. Indeed, it has been noted that tyloses appeared to hinder, but not entirely block, the movement of radiolabelled amino acids in the xylem sap at the ligule of senescent leaves of Lolium temulentum (Chaffey and Pearson, 1985). However, the roles of drying, cavitation and tylosis as processes within the syndrome of senescence, and concomitant effects on an essentially passive long-distance transport system, have not previously been investigated—despite the water status of grass propagules potentially having considerable ecological and economic implications (Lee and Harmer, 1980). Although the glumes and lemmae of all grasses tested to date are capable of gas exchange (Porter et al., 1950; Thorne, 1966; Ong and Marshall, 1975; Ong et al., 1978), leafy spikelets or ‘plantlets’ of pseudoviviparous species may be ideally suited for the investigation of transpiration-driven water movement. The propagules of these predominantly arctic/alpine grasses consist of indeterminate spikelets, which revert to vegetative growth before dehiscing from the parent plant. These propagules are capable of photosynthesis (Lee and Harmer, 1980; Pierce, 1998) and produce adventitious roots, rapidly becoming established after wind or water dispersal; the speed of establishment giving them an advantage over seeds in short arctic/alpine growing seasons (Lee and Harmer, 1980). However, water supply to plantlets during their development may be of critical importance to this reproductive strategy, as older plantlets are prone to water stress (Lee and Harmer, 1980), thereby potentially restricting the range of these species.
The hypothesis tested was that transpiration flow to developing propagules of P.alpina var. viviparara L. via the culm is not fully restricted during its senescence.
In leaf tissue, the first outwardly visible signs of senescence are declining rates of photosynthesis and loss of chlorophyll. This is apparent initially as direct degradation of photosynthetic pigments and, in the later stages of senescence, as degradation of the chloroplast (Gepstein, 1988). It is likely that chloroplast degradation and protein turnover processes in senescent, non-lignified plant organs may follow a common pattern, but that the rate and duration of the events involved may differ between organs and biotypes (Steinitz et al., 1980; Debata and Murty, 1981, 1982; Seo et al., 1981). In the present study, declining photosynthetic pigment content and degradation of chloroplasts were used as indicative of the extent of senescence within the inflorescence, and provide a context in which to consider the operation of the transpiration stream.
Both bright-field microscopy and dark-field detection of a tracer, fluorochrome, in the transpiration stream were used to quantify tylosis and cavitation, respectively, in culm tissues at different stages of development. Descriptions throughout follow the synflorescence concept as applied to grasses (i.e. that the overall reproductive architecture is composed of a series of similarly organized co-florescences; Vegetti and Anton, 1995; cf. Fig. 1 for a diagrammatic representation of the system studied).
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Plant growth and nutrient regime
Plantlets of a biotype of Poa alpina were obtained from the Hohe Mut ridge, Oetztal, Austria (46° 50' 12'' N, 11° 2' 50'' E) at an altitude of 2641 m above sea level. A more specific identification of biotype was not possible via cytological techniques, as a range of chromosome numbers may be apparent even within single root-tips of Poa alpina (Müntzing, 1980
), resulting in differing nuclear DNA contents between root-tips and between sibling plants (Steiner et al., 1997). All experiments described in the present paper utilize this single biotype of P. alpina. Nomenclature of grass follows Hubbard (Hubbard, 1984).
Plants were grown in washed silver sand (William Sinclair Horticulture Ltd., Firth Road, Lincoln, UK) in 1.0 l capacity pots. Nutrients were supplied as a one-fifth strength Long Ashton nutrient solution (Hewitt, 1966). In addition, phosphate (as NaH2PO4.2H2O) and nitrate plus ammonium (as NH4NO3) were provided at final concentrations of 0.6 and 1 mg equivalent l-1, respectively. Nutrients were applied every second day, until the nutrient solution fully saturated the pot. Pots were washed through with tap water on alternate days in order to avoid concentration of available nutrients in the growth medium resulting from evaporation.
A period of vernalization was required for initiation of synflorescence production (Pierce, 1998). An alpine greenhouse was used to house young plants over winter months in chilling temperatures (0.9±0.6 °C minimum and 15.0±0.9 °C maximum averaged over January to April, 1998; n=20) and natural daylight (short daylength). When required, batches of plants were moved to a heated greenhouse (11.7±0.7 °C minimum and 28.5±1.5 °C maximum, January to April, 1998; n=20). Natural daylight was supplemented with 400 W high pressure sodium lighting (Thermoforce Ltd., Heybridge, Maldon, Essex, UK) to provide 16 h daylength. The time of exsertion of the paracladial zone (panicle) was defined as the date at which the main florescence (spikelet) became visible at the ligule of the youngest leaf (i.e. when the spikelet was no longer surrounded by the leaf sheath). On exsertion the pseudostem was tagged with the date.
Components of the synflorescence axis
The distance between the ligules (interligular distance) of the five youngest leaves on the main axis of six replicate plants was measured twice per week. At exsertion of the main florescence, the distance between the base of the main florescence and the ligule of the youngest leaf was measured until the entire paracladial zone had emerged. From this point onwards the length of the rachis, and also the length of the visible peduncle, were measured. Culms were supported during later stages of growth by canes in order to prevent folding and collapse.
Throughout reproductive development, plants were harvested 1 h after watering and the paracladial zone, the distal internode of the culm, and also the youngest fully expanded leaves of two non-flowering tillers were removed (cf. Fig. 1
). The paracladial zone was divided into distal and proximal halves by spikelet number (Pierce, 1998), and all green material separated from visibly senescent material, with only green material being used. The distal internode of the culm (peduncle) was divided longitudinally (one half being used immediately for determination of photosynthetic pigment content, as detailed below). The fresh weight of all excised plant material was determined and plant material was then oven-dried to constant weight. Absolute water content was calculated on a dry weight basis.
Determination of photosynthetic pigments
Chlorophyll a and b and carotenoid content of the distal internode of the culm were determined after the method of Lichtenthaler and Wellburn (Lichtenthaler and Wellburn, 1983). The total photosynthetic pigment content of plant material was initially calculated on a fresh weight basis. Using the absolute water content of the reciprocal half of the internode, the dry weight of the material used in pigment analysis was estimated, and the total photosynthetic pigment content presented on a calculated dry weight basis in order to avoid the complications of possible changing water content of tissues.
Anatomy of the culm
A modified version of the anatomical technique described previously (Lo Gullo and Salleo, 1991) was used to quantify the degree of cavitation in the xylem of the culm. Reproductive shoots of two ages were used (20 d and 40 d from exsertion of the paracladial zone). Shoots were excised from the roots at the root/shoot interface (an initial study having revealed that fluorochromes did not move beyond the root/shoot interface of intact Poa alpina). Excision was carried out under water to avoid breakage of the transpiration stream. Tillers were also excised, leaving just the entire main axis as the unit of study. The cut end of the shoot was then placed into 2 ml of 1% (w/v) lucifer yellow dithionite (LYCH; Oparka and Read, 1994) and control material placed in 2 ml of distilled water. All plants were left for a period of 1 h in a controlled environment room at 15 °C and PPFD of 250 µmol m-2 s-1 (PAR) at the leaf surface, after which the main axis was rapidly dissected into its component parts: (a) the basal node of the culm, (b) a 1 cm length of the basal internode of the pseudostem, (c) the distal-most node of the culm, (d) a 1 cm length of the distal-most internode taken from immediately proximal to the paracladial zone, and (e) plantlets and their supporting pedicels.
Material was fixed, under darkened conditions, in immunofix and embedded in Paraplast wax. Transverse sections of 10 µm thickness were cut and mounted. Slides were viewed with a Diaphot TMD-EF inverted microscope (Nikon UK Ltd., Telford, Shropshire, UK) using an HBO 100 W/2 mercury short-arc lamp (Osram Ltd., Wembley, Middlesex, UK) as a near ultra-violet light source. The blue-violet (BV) excitation method was used. The extent of autofluorescence within tissues was determined by visual comparison with unstained control material (Koch, 1972).
Cavitation
The number of vascular bundles in which fluorochrome was present was compared with the number in which fluorochrome was completely absent in order to calculate an index of cavitation. The mean indices of younger and older material and of different types of vascular bundle were then compared using Analysis of Variance (ANOVA).
Occlusion of xylem vessels
Serial sections of the main axis, again of 10 µm, were stained with toluidine blue (0.05% (w/v) in benzoate buffer) (Bolhàr-Nordenkampf and Draxler, 1993) and dried prior to mounting with Canada balsam. Slides were viewed in bright field on a Diaphot TMD-EF inverted microscope and the presence and position of tyloses noted. The length of occlusions in xylem vessels was calculated by multiplying section thickness by the number of sections in which the occlusion occurred. An index of occluded to unblocked vessels was calculated, with an occluded vascular bundle being defined as a vascular bundle in which one or more elements were either fully or partially blocked.
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Reproductive phenology
During reproductive growth, the pseudostem elongated by virtue of the successive lengthening of the distal two interligular portions (i.e. including stem internodes and leaf sheaths) (Fig. 2
). Interligular distances proximal to this remainined short (interligule 5 (proximal) ceasing extension at a mean length of 2.17±0.44 mm, and interligule 4 at 3.17±0.5 mm (n=6)). The distal internode of the culm (i.e. the peduncle) was visible 9 d after exsertion of the main florescence, at which time the paracladial zone was fully exserted and the rachis fully extended. Extension growth ceased sequentially in each interligule, followed by cessation of culm extension growth by 30 d. At this point the entire synflorescence had achieved a length of 396±40 mm and the culm was observed to be yellow rather than green, with plantlets readily shedding. In unsupported plants grown alongside experimental replicates the culm did not readily collapse before this point, but was prone to collapse after, but not necessarily at, this point in development. Plantlets retained green leaves throughout development, but ‘blasting’ or ‘whitehead’ was apparent in older plantlets, as glumes and older plantlet leaves senesced.
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Tissue water content
The absolute water content of the peduncle declined from 500% to 0% over a 52 d period (Fig. 3a). Absolute water content of green material in the distal and proximal halves of the paracladial zone were not significantly different (P=0.73, as determined by Student's t-test), and declined from approximately 450% to 0% over a period of 55 d after exsertion (Fig. 3b). The youngest fully expanded leaves of non-flowering tillers showed no change in absolute water content during the reproductive development of the main axis, remaining at approximately 220% (Fig. 3c).
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) and distal (
)) during reproductive development and (c) the youngest fully expanded leaf of non-flowering tillers during reproductive development of the main axis. Data points represent individual measurements (n=30 in all cases). Equation of the fitted line in all cases is: y=yo+ax+bx2+cx3. (a) r2=0.79, P
Tissue photosynthetic pigment content
A P value of less than 0.001 denoted that there was a strong tendency for peduncle photosynthetic pigment content to decline with time (from 0.2 mg g-1 DW (calculated) at paracladial exertion to 0.02 mg g-1 DW (calculated) at 50 d from exertion), despite photosynthetic pigment content of younger tissues being highly variable (Fig. 4).
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Cavitation
Fluorochrome was visible in all vascular bundles of all replicates at 20 d after exsertion. At 40 d after exsertion, fluorochrome was present in 92.3±7.7% of major vascular bundles and 62.3±19.9% of minor vascular bundles (Table 1), with a significant difference between means over time (P
0.05; Table 2a), but not between the two types of vascular bundle. Photomicrographs of transverse stem sections from these two developmental times can be seen in Fig. 5 (A, B). Chlorenchyma and also stomata were observed in culm internodes 20 d after exsertion (Fig. 5A, C), although at 40 d after exsertion no chloroplasts were present (inferred from the lack of red fluorescence in Fig. 5A compared to Fig. 5B). Fluorochrome was present in plantlet tissues (pedicel, glumes, leaf sheaths, and amphistomatic blades (Fig. 5D)) at both stages of development. Fluorochrome was present throughout the nodal plexi at both stages of development (Fig. 5E, F).
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Occlusion of the vasculature
No occlusions were found in the peduncle, distal node or in plantlet material, at any time over the developmental period studied. Occlusions were occasionally observed in the protoxylem of vascular bundles from the culm internode immediately proximal to the basal node (seen in transverse section in Fig. 6). Occlusions infrequently extended into the node, but not into the nodal plexus. Such occlusions, when measured in longitudinal section (not shown) ranged from 40 µm in length (Fig. 6C), through 500 µm (Fig. 6A) to 640 µm (Fig. 6B). They were not apparent at 20 d after exsertion. At 40 d after exsertion, occlusions were detected in 21.9±12.7% of major vascular bundles, and 12.7±7.5% of minor vascular bundles (Table 1). There was a significant increase in the frequency of occlusion over time (P0.05; Table 2b), but not between the two types of vascular bundle.
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Discussion |
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A decline in photosynthetic pigment content in the culm began from the moment of paracladial exsertion, indicating that senescence processes in the culm were in operation from an early stage of development, i.e. while the culm was initially elongating. Also, the complete lack of chloroplasts in culm tissues at 40 d indicates that senescence of the culm was particularly advanced by this stage. The ‘blasting’ or ‘whitehead’ (senescence in the grass synflorescence associated with drying of tissues) in the paracladial zone observed at this time was a visual indication of an inadequate supply of resources via the xylem of the culm, as ‘blasted’ or desiccated glumes have been correlated with relative water contents below 50% and water potentials of below -3 MPa in rice (Oryza sativa cv. IR36; O'Toole et al., 1984
), but are also a general symptom of nutrient stress (Marschner, 1995). Also, water stress is evident in the older plantlets of pseudoviviparous grasses (including Poa alpina) as increased concentrations of the compatible osmoregulatory solute proline (Lee and Harmer, 1980). As water content of the youngest fully expanded leaf on non-flowering tillers remained at approximately 220% (on a dry weight basis) throughout the present study, and plants were grown under a strict watering regime, it is evident that the plant as a whole experienced little change in water availability, and that declining water content and concomitant water stress were inherent to the developing synflorescence. It should be noted that, during culm development, it is not only the mechanical properties of the cells that change. Hydraulic relations may also change as a result of altered ‘wettability’, which, in turn, will have significant implications for water supply via the culm. A detailed study of this possibility was beyond the scope of the investigation reported here.
Fluorochrome was not detected at the stomata of the culm after 1 h, indicating that transpirational demand for water by this organ was minimal over this period. The declining water content of culm tissues may therefore be the result of membrane degradation and an inability of cells to retain water during senescence (Chaffey, 1983). Here a distinction must be made between water loss from the yellowing culm and from green plantlet tissue which was clearly at a different developmental stage; any similarities in the pattern of water loss may well be coincidental.
Despite declining water content of the synflorescence, transpiration flow via the culm was maintained throughout the period studied, and was little hindered by barriers such as embolism or tylosis, with plantlet stomata driving transpiration flow even at a time when plantlets readily dehisced. Thus a continued physiological connection existed throughout the development of plantlets, supporting the hypothesis that plantlets may acquire more resources (at least in terms of mineral nutrition) from the parent plant the longer they remain attached (Harmer and Lee, 1978a). The data also support the suggestion of Lee and Harmer (Lee and Harmer, 1980) that as plantlets grow, their demand for water gradually exceeds the physical capacity of the culm to supply it. This is currently being further elucidated by direct measurement of xylem tensions and fluxes over time. Such an approach might also help further explain the low frequencies of cavitation and tylosis detected in the present study; presumably a continued transpiration flow, high water availability and locally high water contents in the xylem prevented both cavitation and the in-growth of tyloses, and explain their low frequencies throughout development of the culm.
The vascular bundles of the grass culm and rachis are continuous between internodes (Joarder and Eunus, 1980), with nodal plexi physically connecting these vascular tissues at the node (Arber, 1930; Hitch and Sharman, 1971). In the present study, fluorochrome was shown to move throughout nodal plexi, demonstrating a physiological connection in terms of water transport. Hence cavitation in proximal internode vessels will not necessarily result in dysfunctional tissue throughout more distal lengths of the culm, as water movement via plexi can bypass dysfunctional vessels. In addition, xylem recovery from cavitation may also potentially decrease the impact of cavitation on transport (Kramer and Boyer, 1995; Salleo et al., 1995; Sperry et al., 1988a, b; Tyree and Sperry, 1988), indeed, xylem recovery of water-stressed maize (Zea mays) may occur in a single night (Tyree et al., 1986) although the permanence of individual embolisms was not investigated in the present study.
It is clear that the cessation of allocation to pseudoviviparous plantlets via the xylem of the culm is only likely to occur with catastrophic breakage of physical connections; either via propagule dehiscence or the collapse of the culm. The eventual collapse or ‘lodging’ of the culm is thought to be an advantage to pseudoviviparous grasses as it places the plantlets into contact with the substrate en masse and possibly facilitates colonization via extensive rooting and soil stabilization (Harmer and Lee, 1978b). In the present study lodging was not observed until late in development (i.e. after the cessation of culm elongation) in unsupported plants, and was not the consequence of exceeding a critical buckling length (Niklas, 1992, 1994). The timing of lodging is possibly dependent on both the growth of propagules (i.e. increased bending moment acting on the culm; Silk et al., 1982), and decreased water content of culm tissues over time, acting to decrease turgor and thus flexural rigidity (Niklas, 1991, 1992). Thus lodging is perhaps inevitable as indeterminate plantlets grow (Pierce, 1998) and exceed the mechanical threshold of the culm, and/or as the mechanical threshold changes as a response to declining water content during senescence.
In natural surroundings, changing wind speeds produce additional dynamic loads on stems, which may perhaps act to cause lodging at an earlier time during culm senescence. However, gusting of wind and oscillatory movement is more effective in providing the shear forces necessary for the dehiscence of fruits than high and constant wind speed (Niklas, 1992), and may potentially facilitate the dehiscence of grass propagules. Thus, in P. alpina, it is possible that the biomechanical response of the culm to water content during senescence, by determining the length of time over which propagules remain attached, is of critical importance to pseudoviviparous grass reproduction, in addition to the direct effects of water content per se.
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Acknowledgments |
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SP was supported by a University of Durham Studentship in collaboration with the Institute of Terrestrial Ecology, Bangor Research Unit. We thank Howard Griffiths for useful comments on the manuscript, and to Jackie Spence and Dorothy Catling for histological experience and advice.
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3 To whom correspondence should be addressed. Fax: +44, 191 374 2417. E-mail: Robert.Baxter{at}durham.ac.uk
4 Present address: Department of Agricultural and Environmental Sciences, University of Newcastle upon Tyne NE1 7RU, UK.
5 Present address: School of Agriculture and Forest Sciences, University of Wales, Bangor LL57 2UW, UK.
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S. PIERCE, C. M. STIRLING, and R. BAXTER Pseudoviviparous Reproduction of Poa alpina var. vivipara L. (Poaceae) during Long-term Exposure to Elevated Atmospheric CO2 Ann. Bot., May 1, 2003; 91(6): 613 - 622. [Abstract] [Full Text] [PDF]
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 S. Pierce, C.M. Stirling, and R. Baxter Architectural and physiological heterogeneity within the synflorescence of the pseudoviviparous grass Poa alpina var. vivipara L. J. Exp. Bot., October 1, 2000; 51(351): 1705 - 1712. [Abstract] [Full Text] [PDF]
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