Sieve Elements: Comparative Structure, Induction and Development

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We hypothesized that non-collapsed late phloem sieve tubes formed in the previous growing season remain functional for a short period at the beginning of the next growing season, in order to help the overwintered and newly developing phloem elements to translocate a sufficient amount of photosynthates to the locations of active growth i. In addition, differences in the ultrastructure of the sieve tubes formed in the current and previous growing seasons may reveal structural differences, such as callose deposition on sieve plates and accumulation of phloem-protein P-protein which affects their functionality.

The study was conducted at two uneven-aged mixed beech F. The site Panska reka PAN— m above sea level a. A detailed description of the site is presented in Prislan et al. The samples collected at this site were used for intra-annual phloem formation analysis with LM in Both forest sites belong to the Blechno-Fagetum forest association, with F. The first site is managed by sustainable forest practices, while the second is left to natural development. The climate at the sites is humid continental. According to the climate record for the period —, the mean annual temperature is In , the average annual temperature and amount of precipitation were above the long-term average; At PAN, six dominant or co-dominant, healthy F.

The estimated age of the trees at PAN was years.

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Microcores of stem tissues were collected at weekly intervals between 21 March and 31 August , using a Trephor tool Costruzioni Meccaniche Carabin C. The samples were collected at breast height 1. To avoid wound effects, sampling locations were separated by 10 cm. Each micro-core contained phloem non-collapsed and collapsed , vascular cambium and at least two of the last-formed xylem growth rings.

The sample preparation procedure is described in detail in Prislan et al. The prepared cross-sections were used for bright field imaging with a Leica DM microscope Leica Microsystems, Wetzlar, Germany using transmission light.

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The number of cambial cells and the widths of the current developing phloem increments were measured for three radial files in each histological section, to evaluate the duration of cambial cell production and the dynamics of early EP and late phloem LP formation. Similarly, the widths of early pEP and late phloem formed in the previous year pLP were measured to evaluate the dynamics of sieve tube secondary changes in relation to the phloem formed in the current year. Early and late phloem were distinguished based on different sieve tube size, separated by a tangential band of axial parenchyma cells Prislan et al.

Intra-annual increases in phloem widths were fitted to the Gompertz function to evaluate the date of maximum phloem increment Rossi et al. The day of the year DOY was recorded for the phenological phase of cambial activity and phloem formation, as well as secondary changes in the phloem increments: i beginning of cambial cell production BCP , ii cessation of cambial cell production CCP , iii maximum phloem cell production PHmax , iv transition from early to late phloem tELP , v fully collapsed late pLPc phloem formed in the previous year and vi beginning of current year early phloem sieve tube collapse EPc.

In spring and autumn, the dates of leaf unfolding LU and autumnal leaf colouring LC were recorded for selected trees, as described in Prislan et al.

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For each phenological phase growing degree days GDD and average mean temperature day before the occurrence of each event were calculated see Prislan et al. The samples were taken at a spacing of at least 10 cm to avoid wound effects. The samples were collected on 6 March, 3 April and 19 June to investigate the ultrastructural changes in phloem and cambial cells before and during cambium reactivation, and at the culmination of daily radial stem growth.

The sampling dates were selected based on our previous observations of intra-annual xylem and phloem formation at the same sites Prislan et al.

In addition, the ultrastructure of sieve plates and callose deposition in sieve tubes in the youngest two phloem increments was examined to decide on their non functioning. The samples contained cambium and the youngest xylem and phloem tissues. To observe the ultrastructural seasonal changes in the cambium and inner phloem, the pieces were fixed in 3.

After a few hours, the tissue samples were transferred to a fresh fixative solution in the laboratory. The parallel samples were either fixed for an additional 2 h at room temperature on a rotor or were subjected to microwave-assisted fixation. The following day, the samples were washed three times for 25—30 min in 0. Semi-thin 0. Since no major differences in the ultrastructure were observed between the conventionally fixed samples and the samples subjected to microwave-assisted fixation, they are not presented separately in the Results section.

Scanning electron microscopy was used to observe the three-dimensional anatomical characteristics of sieve plates in the transverse and end walls of the sieve tubes of the youngest two phloem increments. Seasonal changes in the phloem increment formed in the previous year and current phloem increment safranin-astra blue staining. Observed phases of phloem formation in growing season at Panska reka in relation to weather conditions. The occurrence of the phases is recorded as day of the year DOY.

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Leaf colouring LC occurred 11 weeks later, i. At the date of the first micro-core sampling on 21 March , the cambium was still dormant and composed of three to four cell layers.

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At that time, early phloem sieve tubes formed in the previous year pEP were partly collapsed. In contrast, late phloem sieve tubes formed in the previous year pLP appeared to be non-collapsed, as indicated from their unchanged shape and size Figure 1 a. The collapse of older phloem is a progressive process, which continuously occurred during the sampling period Figure 2. However, in most trees, pLP was not completely collapsed after the end of the current growing season. The rates of increase of the width of non-collapsed phloem and the width of the current phloem ring were similar.

At that time, the current phloem increment was composed of a developing early phloem part only. In the samples collected on 6 March, the cambial cells displayed thicker cell walls than those of active cambial cells and dense abundant cytoplasm, with numerous small vacuoles and large lipid droplets indicating the dormant state of the cambium.

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The youngest phloem could be divided into three parts: i two to three layers of undifferentiated, overwintered phloem cells adjacent to the cambium, ii non-collapsed pLP and iii partly collapsed pEP Figure 3 a and b. Although overwintered phloem cells were undifferentiated, they could be distinguished from cambial cells by their rounder shape and larger radial dimensions, while their ultrastructure was similar to that of fusiform cambium cells Figure 3 b.

Round sieve tubes in non-collapsed pLP were accompanied by companion cells Figure 3 c. The lumen of sieve tubes was mostly empty, although endoplasmic reticulum and mitochondria were often attached to the cell wall Figure 3 d. The companion cells had abundant cytoplasm containing a few bigger vacuoles and numerous smaller ones. Larger lipid droplets, extensive rough endoplasmic reticulum, numerous mitochondria, a nucleus with nucleolus and plasmodesma in the cell walls were also often observed in the companion cells Figure 3 e.

In general, sieve plates were less frequent in pLP than in pEP sieve tubes.

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Axial parenchyma were more abundant in pLP than in pEP and their appearance differed within the phloem increment. Most axial parenchyma cells had an oval shape, with slightly thicker cell walls than those of sieve tubes Figure 3 f. However, some phloem axial parenchyma cells contained highly electron dense cytoplasm which appeared dark under TEM Figure 3 c.

Light microscope a and TEM micrographs b—f of the cambium and phloem increment formed in the previous year, in samples collected before the resumption of cambial cell production on 6 March Axial parenchyma cells AP often contained electron dense contents. On 3 April, the cambium was in transition from a dormant to an active state. In addition to an increased number of cambial cell layers Figure 4 a , their ultrastructure changed; small vacuoles merged into one large central vacuole and the cytoplasm was compressed against the thin cell walls Figure 4 b.

Newly formed phloem cells were observed adjacent to the cambium, and overwintered phloem cells started to differentiate Figure 4 b. Sieve tubes then started to enlarge and divide, whereby companion cells were created by the formation of new transverse cell walls, which separated the companion cells from the differentiating sieve tubes Figure 4 c. In contrast to changes in fusiform cambial cells, the ultrastructure of late phloem cells of the previous year, i.

Light microscope a and TEM micrographs b—d of the structure of the phloem at the onset of cambial cell production, on 3 April a—c and 19 June d.

Overwintered phloem cells have started differentiation into early phloem cells EP. On 19 June, at the culmination of radial growth, cambium cells were characterized by a large central vacuole and were mostly divided by a newly formed cell plate or thin cell wall, indicating high divisional activity. At that time, the entire EP had been formed, while late phloem development was in progress Figure 1 d.

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The content of the sieve tube lumen was similar to that observed in previous sampling. The ultrastructure of the companion cells in EP slightly differed from that observed in the pLP; although the cytoplasm was dense, the companion cells often contained a large central vacuole, mitochondria and rough endoplasmic reticulum Figure 4 d. Prior to the onset of cambial reactivation on 6 March, sieve plates in the pEP sieve tubes were characterized by larger and fewer pores compared with sieve plates in pLP Figure 5 a—c.

In addition, there were differences in the shape of the pores in sieve plates in transverse and end walls Figure 5 c and d. The sieve plates in older collapsed phloem were never completely occluded by callose.

Moreover, pores in sieve plates in older sieve tubes were open and larger than in younger sieve tubes Figure 6 a and b. In collapsed pEP sieve tubes, phloem-protein P-protein aggregates were less abundant around the sieve plates; however, inter-poral walls were surrounded by a thick layer of callose, covering most of the pores of the sieve plates Figure 7 a and b.

Around the sieve plates in the non-collapsed pLP sieve tubes, P-proteins were dispersed as denser, filamentous material, which blocked the sieve pores Figure 7 c and d.