Complete tylosis formation in a latest Permian conifer stem

Complete tylosis formation in a latest Permian conifer stem

Zhuo Feng1,2,*, Jun Wang2, Ronny Roßler3, Hans Kerp4 and Hai-Bo Wei1

1Yunnan Key Laboratory for Palaeobiology, Yunnan University, Kunming 650091, PR China, 2State Key Laboratory ofPalaeobiology and Stratigraphy (Nanjing Institute of Geology and Palaeontology, CAS), Nanjing 210008, PR China,

3Museum fur Naturkunde, Moritzstraße 20, D-09111 Chemnitz, Germany and 4Forschungsstelle fur Palaobotanik,Westfalische Wilhelms-Universitat Munster, Schlossplatz 9, D-48143 Munster, Germany

* For correspondence. E-mail [email protected]

Received: 6 December 2012 Returned for revision: 3 January 2013 Accepted: 30 January 2013

† Background and Aims Our knowledge of tylosis formation is mainly based on observations of extant plants;however, its developmental and functional significance are less well understood in fossil plants. This study,for the first time, describes a complete tylosis formation in a fossil woody conifer and discusses its ecophysio-logical implications.† Methods The permineralized stem of Shenoxylon mirabile was collected from the upper Permian(Changhsingian) Sunjiagou Formation of Shitanjing coalfield, northern China. Samples from different portionsof the stem were prepared by using the standard thin-sectioning technique and studied in transmitted light.† Key Results The outgrowth of ray parenchyma cells protruded into adjacent tracheids through pits initiallyforming small pyriform or balloon-shaped structures, which became globular or slightly elongated when theyreached their maximum size. The tracheid luminae were gradually occluded by densely spaced tyloses. Thehost tracheids are arranged in distinct concentric zones representing different growth phases of tylosis formationwithin a single growth ring.† Conclusions The extensive development of tyloses from the innermost heartwood (metaxylem) tracheids to theoutermost sapwood tracheids suggests that the plant was highly vulnerable and reacted strongly to environmentalstress. Based on the evidence available, the tyloses were probably not produced in response to wound reaction orpathogenic infection, since evidence of wood traumatic events or fungal invasion are not recognizable. Rather,they may represent an ecophysiological response to the constant environmental stimuli.

Key words: Shenoxylon mirabile, tylose, fossil plant, conifer wood, ecophysiological response, late Permian,China.

INTRODUCTION

In land plants, tyloses are spheroidal protoplasmic bulges thatare generally formed when the adjacent parenchyma cells,axial parenchyma or ray cells, protrude into the dead axial con-ducting cells (Esau, 1965). Tyloses usually extend through thepits of the tracheary cells and have a variety of functions, e.g.occlude the cell cavities blocking water movement throughthem (Pearce, 1996). The process of tylosis formation is com-plicated, and includes numerous metabolic changes, as well asthe supply of quantities of phenolic compounds, lignin andaromatic substances (Mauseth, 2003). Tyloses have been fre-quently seen in extant dicotyledonous angiosperms (Saitohet al., 1993), but they also could be common in other groupsof vascular plants. This is uncertain since relatively fewinvestigations on tylosis occurrence in other plant (non-dicotyledonous) groups have been conducted. Although exten-sive fossil records reveal that tylosis formation commonlyexisted in woody plants since at least the Carboniferous(Scheckler and Galtier, 2003), descriptions and functional ana-lyses of tyloses to date have been obtained almost entirelyfrom modern dicots (Zurcher et al., 1985).

Here we report the earliest complete developmental process oftylosis formation in a conifer stem, Shenoxylon mirabile, fromthe upper Permian (Changhsingian) Sunjiagou Formation in

the Shitanjing coalfield, Ningxia Hui Autonomous Regionof northern China. Comparisons with tylosis formation inmodern plants enable inferences on the ecophysiological roleof the well-preserved tyloses in this fossil plant. The abundanceof tyloses in the wood from the uppermost Permian suggestsinstability of the environment.

MATERIALS AND METHODS

The Shitanjing coalfield fossil locality is situated in the north-ernmost part of the Ningxia Hui Autonomous Region, northernChina (Feng et al., 2011). Tectonically, the Shitanjing coal-field is located in the western Ordos (also known as Erdos orErduosi) sedimentary basin at the north-western edge of theNorth China Block (NCB). The area of the north-westernedge of the NCB is notably rich in well-preserved latePalaeozoic permineralized woody tree stems.

The Sunjiagou Formation in the Shitanjing coalfield isapprox. 80 m thick, representing a river–delta–lake sediment-ary succession, with several pink-coloured volcanic ash depos-its in the lower portion, and a thin bed of lenticular limestonenear the top of the section. The limestone bed is widely recog-nized in the Sunjiagou Formation elsewhere in the NCB. Thebed yielding permineralized material is composed of coarse- to

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medium-grained sandstone with cross-bedding, representing afluvial sedimentary setting (Feng et al., 2011; Feng, 2012).

The silicified stem described in this paper was formallydescribed as Shenoxylon mirabile Feng, Wang et Roesslerand has been suggested to be a conifer (Feng et al., 2011).Thin sections were prepared as follows. First, the specimenwas cut through transverse, tangential and longitudinalplanes into pieces of appropriate size by using a diamondsaw. The top surfaces were sequentially polished on a grindingwheel with carborundum grades of 240, 400 and 800 in turn.The smooth top surface was then glued onto a glass slidewith epoxy resin, and the bottom surface was ground downto a thickness of approx. 30 mm. Most of the thin sectionswere covered with a glass cover-slip using abienic balsam.Optical examination and photomicrographs were undertakenusing a Nikon E50i transmitted light microscope equippedwith a Nikon DXM 1200F digital camera. Composite imageswere stitched together using Adobe Photoshop CS v. 8.0.

The specimen, thin sections and digital photomicrographs arereposited in the Palaeobotanical Collections of the Yunnan KeyLaboratory for Palaeobiology, Yunnan University, PR China,with catalogue number YKLP20005.

RESULTS

The specimen of Shenoxylon mirabile that contains the tylosesis described here. It is approx. 150 mm in diameter, and dis-plays a well-preserved eustele and secondary xylem. Tylosesare recognizable throughout the primary and secondaryxylem. All tyloses are three-dimensionally preserved withinthe tracheids.

In the secondary xylem, tylose-filled tracheids occur in dis-tinct concentric zones within single growth rings. The zones oftylose-free tracheids appear much brighter in transmitted lightthan the intercalated tracheid zones that are densely filled withtyloses (Fig. 1A, arrows). Sometimes the tylose-free tracheidsare irregularly present among the tylose-filled tracheids(Fig. 1B). Within the tracheids, the tyloses usually aredensely spaced and polygonal in shape, occupying the entiretracheid luminae (Fig. 1C). Single tyloses are also observedin cross-sections (Fig. 1D); they show more or less roundedoutlines, with 1.5- to 2-mm-thick walls. Small pyriform struc-tures, commonly ,10 mm in diameter, that protrude from raycells through the pits represent the early stage of tylosis forma-tion (Fig. 1E). The pyriform structures then become somewhatballoon-shaped with narrower bases, but sometimes showirregular outlines (Fig. 1F).

Longitudinal sections of the secondary xylem show tylosesin the tracheids in both the radial and tangential views(Fig. 2A, B). There are different types of arrangement oftyloses within the tracheids. Densely spaced polygonaltyloses may occupy almost the entire width of the tracheids(Fig. 2C), or groups of one to three tyloses are aligned in ver-tical files, reaching from one end of the tracheid to the other(Fig. 2D). These two types of arrangement usually occur indifferent tracheids (Fig. 2E). Isolated spheroidal to ellipsoidaltyloses are present and are up to 27 mm wide and 38 mm long(16–27 mm wide × 19–38 mm long; n ¼ 50) (Fig. 2F). Thetyloses decrease in diameter toward the tapering tip of the trac-heids (Fig. 2G, H). Uniseriate bordered pits occur singly or in

rows on the surface of radial tracheid walls (Fig. 3A, B).Tangential sections also show that balloon-shaped tyloses pos-sessing narrow bases (Fig. 3C). A single ray cell can protrudeinto more than one tracheid (Fig. 3D, arrows); however, asingle tracheid can receive tyloses from more than one raycell (Fig. 3E). Ray cells and tylosis initials commonlycontain amorphous black substances (Fig. 3F). Tyloses arealso present in the primary xylem tracheids (Fig. 3G, H,arrows).

The dimension and shape of the ray cells that produce tyloseare no different from the non-tylose-producing ray cells.

DISCUSSION

A conspicuous feature of our conifer wood is the highly devel-oped tyloses in the tracheids through the primary to the sec-ondary xylem. Tyloses have been documented from diversefossil plant groups, including progymnosperm (Scheckler andGaltier, 2003), ferns (Williamson, 1877, 1880; Weiss, 1906;Phillips and Galtier, 2005, 2011) and angiosperms (Bancroft,1935; Spackman, 1948; Brett, 1960; Manchester, 1983;Nishida et al., 1990; Poole and Francis, 1999; Prive-Gillet al., 1999; Meijer, 2000; Poole and Cantrill, 2001; Teradaet al., 2006; Nishida et al., 2006; Castaneda-Posadas et al.,2009). Except for some sporadic records of tylosoid occlusionsin the resin canals of fossil conifers (Jeffrey, 1904; Holden,1915; Ogura, 1944, 1960; Nishida et al., 1977; Robison,1977; Nishida and Oishi, 1982), there are relatively fewreports concerning tyloses in fossil conifers. A complete de-velopmental study on tylosis formation in Palaeozoic conifershas not been reported to date.

The first report of tylose structure in fossil conifers is ofPityoxylon succinifer, preserved in Oligocene Baltic amber(Conwentz, 1889). Although the classification of this wood isstill debated, and it has been assigned to Pinites (Goppert,1841) and Pinus (Conwentz, 1889). The occlusions in the trac-heids are widely accepted as being tyloses (Seward, 1919,p. 230; Ogura, 1960). Tyloses were also noted in the Jurassicconifer Metacedroxylon scoticum from Scotland (Jordan,1914), the Late Jurassic conifer Protocedroxyion arancarioidesfrom Spitzbergen (Gothan, 1910) and the Late TriassicAraucarioxylon sp. from Vietnam (Colani, 1919); however,these early reports of tyloses were not further discussed.

Abundant septum-like structures in the tracheids of theJurassic conifer wood, Xenoxylon latiporosum, have been pre-viously interpreted as tracheid membranes by Gothan (1910)and Shimakura (1936). Ogura (1944) suggested that theseseptum structures are tyloses. Due to the co-occurrence ofboth septum and spheroidal/ovoid structures in the tracheidsof X. latiporosum from Korea, Ogura (1944) speculated thatthe horizontal septa could be derived from globular tyloses.Other specimens of the same species from the LowerJurassic of Japan also show similar septa in the tracheids,but they are more pyriform (Watari, 1960). Unlike thoseseen in our material, the thin septae are commonly horizontalin the tracheids of X. latiporosum. Arnold (1952) explained thetracheid septa as bars of Sanio (crassulae), and suspected theirorigin as tyloses, based on similar material from northernAmerica (Medlyn and Tidwell, 1975).

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Ogura (1960) described two new species of Araucarioxylonwith tyloses from the Triassic and Cretaceous of Japan. Theshape of the tyloses in both species varies from pyriform toseptate. Therefore, Ogura (1960) further developed his previ-ous assumption that ray cells protrude through the pits intothe tracheids, first forming small pyriform structures, thenthe pyriform structures enlarged in both directions, and even-tually the septae formed by fusion of the walls of adjacentpyriform structures. The frequent appearance of septae mayresult from the high ratio of ray cells to tracheids in thewood (Watari, 1960). In our material, the individual tylosesare balloon-shaped, spheroidal, or sometimes slightly ovoidwith curved ends. So far, no membranous thin septa havebeen observed in our material.

‘Bud’ and balloon-like structures occurring in the tracheids ofthe conifer stem, Australoxylon mondii, were illustrated from the

upper Permian of the Antarctic (Weaver et al., 1997). The small‘buds’ were interpreted as an early stage of tylosis formationsince the ray cells protruded into the tracheid lumen, and thenthe ‘buds’ expanded into balloon-like structures. Both ‘buds’and balloon-like structures in the Antarctic material are verysimilar to those in our material. Due to the fact that only onethin section shows a few tylose structures, a complete sequencepresenting the progression of tylosis formation could not beestablished in the Antarctic material (Weaver et al., 1997).

Recently, tylosis formation was reported from an EarlyJurassic permineralized conifer axis from Antarctica (Harperet al., 2012). Because of the co-occurrence with fungi in thisstem, it seems possible that the tylosis formation was a re-sponse to fungal infection of a wood rot fungus and servedto build up mechanical barriers against the advancinghyphae. Three developmental stages have been recognized

B

CA

D E F

FI G. 1. Shenoxylon mirabile from the upper Permian Sunjiagou Formation, Shitanjing coalfield, northern China. (A–D, F) Transverse sections: (A) tylose-filledtracheids in a concentric zonate distribution (arrows indicate the tylose-free tracheids in the middle of the image which appear brighter in transmitted light); (B)tylose-free tracheids irregularly distributed within the zones of tylose-filled tracheids; (C) close-up of densely spaced tyloses in tracheids; (D) isolated tylosesshowing spheroidal or ellipsoidal shape; (F) a tylose sometimes shows an irregular outline. (E) Tangential longitudinal section showing a small pyriformtylose growing out from the parenchymatous ray cell through a pit. Scale bars are as indicated on the images. Specimen and thin sections illustrated in thispaper are housed in the Palaeobotanical Collections of the Yunnan Key Laboratory for Palaeobiology, Yunnan University, with catalogue number YKLP20005.




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based on the dimensional and morphological features of thetyloses in the Antarctic stem. The three stages are verysimilar to the early developmental levels of tylosis formationin our material. However, at the final stage of our material,tyloses are further developed and tightly crowded together,whereas in the Antarctic stem, the fully developed tylosesare still somewhat globular and apart from each other. Our ma-terial is very well preserved with great detail but no fungalhyphae were observed in our specimen. Therefore, we canexclude the possibility that the prominent tyloses in our mater-ial have been induced by fungal invasion or fungal infection.

It is worth mentioning that in the progymnospermProtopitys buchiana from the lower Carboniferous of France(Scheckler and Galtier, 2003), the polygonal tyloses denselycrowded in the tracheid luminae resemble those of the lateststage of tylosis formation in our material. Because thesetyloses commonly occur near the growth ring boundaries,Scheckler and Galtier (2003) suggested that the tylosis forma-tion may be caused by the local dormancy water stress.Periodic water shortage is a common phenomenon in manyterrestrial ecosystems. The tylose-filled tracheids in our speci-men are obviously arranged in concentric zones. However,

A

C D E

F G H

B

FI G. 2. Shenoxylon mirabile from the upper Permian Sunjiagou Formation, Shitanjing coalfield, northern China. (A–G) Radial longitudinal sections: (A, B)successive fields showing tracheids in the tylose-filled wood zones; (C) densely spaced tyloses in the tracheids; (D) vertically aligned tyloses in tracheids;(E) densely spaced and vertically aligned tyloses in isolated tracheids; (F) isolated tyloses showing spheroidal or ellipsoidal shapes; (G) vertically alignedtyloses near the end wall of tracheids which have a smaller diameter. (H) Tangential longitudinal section showing tyloses with a smaller diameter toward the

tapering ends of the tracheids. Scale bars are as indicated on the images.




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several tylose-filled wood zones are recognized within a singlegrowth increment. It is possible that the tree lived in anenvironment characterized by constant water stress.

Observations on tylosis formation in extant species revealthat they may be triggered by various kinds of heterogeneityin both abiotic and biotic stimuli, including mechanical injur-ies, infection by pathogenic microorganisms (Biggs, 1987;Pearce, 1990), natural senescence (Dute et al., 1999), heart-wood formation (Chattaway, 1949; Meyer, 1967; Panshin

and DeZeeuw, 1980; Parameswaran et al., 1985; Wilson andWhite, 1986), frost (Cochard and Tyree, 1990) and flooding(Davison and Tay, 1985). Although there are several assump-tions and interpretations concerning tylosis formation inresponse to special environmental conditions, a general ex-planation as to when and how tyloses are produced in responseto different chemical and physical stress factors imposed bythe environment has not yet been given (Sun et al., 2006,2007). However, recent evidence indicates that ethylene

A B

EDC

F G H

FI G. 3. Shenoxylon mirabile from the upper Permian Sunjiagou Formation, Shitanjing coalfield, northern China. (A, B) Radial longitudinal sections of second-ary xylem in the same area in different focal planes, showing bordered pits on the radial surface of tracheids (A) and the tyloses inside the tracheids (B). (C–F)Tangential longitudinal sections of the secondary xylem: (C) single spheroidal tylose shows a narrow base; (D) single ray cell protrudes into different tracheids(arrows); (E) multi-tyloses emerging from the ray cells through the pits into single tracheid; (F) ray cells and tylosis initials commonly contain black substances.(G, H) Radial longitudinal sections of pith and primary and secondary xylem: (G) densely spaced tyloses (arrow) occurring in the innermost portion of the heart-wood; (H) densely spaced tyloses (arrow) in the tracheids of the primary xylem. Abbreviations: PX, primary xylem; SX, secondary xylem; PTX, protoxylem;

MX, metaxylem. Scale bars are as indicated on the images.




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biosynthesis plays an important role in tylosis formation (Sunet al., 2007; McElrone et al., 2010).

The development of tyloses has been regarded as a normalphysiological process marking the transformation fromsapwood to heartwood in many hardwood species (Leitchet al., 1999). However, the tylose-filled tracheids in our mater-ial occur from the innermost heartwood through the outermostof sapwood. Therefore, it is highly unlikely that the tylosis for-mation in our specimen would be a response to heartwoodformation.

Murmanis (1975) cut samples from Quercus rubra and inves-tigated the number of hours required for tylosis formation. Inspring it took 6 h, but during active growth in summer only2.5 h were required. During dormancy, 1.5 months or longerwere necessary for tyloses to appear despite temperatures condu-cive to metabolism. The frequent tylosis formation within asingle growth ring in our specimen might possibly indicate rela-tively rapid environmental changes.

Evidence for the presence of a wide variety of environmen-tal stress factors, including sustained wind, water stress, ele-vated atmospheric CO2 concentration and wildfire, has beenfound based on palaeobotanical data from the upper PermianNCB (Wang and Zhang, 1998; Wang and Chen, 2001), aswell as on a global scale during this critical period (Shenet al., 2010, 2011). According to climatic models, the NCBwas subjected to a relatively long rainfall season in its southernpart, whereas its northern part was dry (Fluteau et al., 2001).The fossil locality of the Shitanjing coalfield is situated inthe western Ordos Basin, on the north-western edge of theNCB. Our specimens were collected from the uppermost partof the Sunjiagou Formation, being late Changhsingian inage. It is therefore very compelling to invoke a relationshipbetween the uncommon repeated reaction of perennialwoody trees and major environmental changes. Additionally,false rings are very commonly present in our wood, andother woods from the same bed, also indicating severe envir-onmental fluctuations (Feng et al., 2011; Feng, 2012).

The massive development of tyloses would effectively slowdown (or even prevent) water transport, and thus may beviewed as a response or adaptation to the environmentalchanges that were common in this terrestrial ecosystem.Axial xylem parenchyma cells are irregularly distributed inthe fossil conifer stems, but a development of tylose fromaxial parenchyma was not observed. Only the ray parenchymacells can account for the capacity of tylosis formation in ourmaterial. Due to the lack of evidence of wound healing andthe repeated formation of tylose-containing wood, we believethat tylosis formation was not induced by mechanical injury.

Conclusions

Wood is known to be a very sensitive indicator of environ-mental change. The anatomical particularities of our materialfrom northern China may provide a rare opportunity toassess how land plants responded or adapted to environmentalchanges during the late Permian.

The complete development of tylosis formation can beobserved in our conifer stem, i.e. the outgrowth of ray cellsprotruding into the adjacent tracheids through the circular bor-dered pits and forming balloon-shaped buds, which then

became globular or slightly elongated and reach theirmaximum diameter. With increasing number and size of thetyloses, the tracheid luminae were gradually occluded.

The abundance of tyloses in our permineralized wood mayindicate that the tree was living in a time interval of extremeecological conditions, in which plants had to develop specialstructures to adapt to the frequent changes of the environmen-tal conditions. Repeated tylosis formation in a perennialwoody plant may indicate an adaptation of these plants to astressful environment. The development of false rings in thesame plant is interpreted as further indication of frequent en-vironmental changes (Feng et al., 2011; Feng, 2012).However, further studies of fossil woods from the same strati-graphic level in other regions are necessary to prove the sig-nificance of our current assumptions and to show theinterrelatedness of ecology, plant physiology and anatomysome 250 million years ago.

ACKNOWLEDGEMENTS

We would like to dedicate this paper to Prof. Herbert Sub (for-merly Museum fur Naturkunde Berlin) at the occasion of his92th birthday. We thank Prof. Zhi-Yan Zhou (NIGPAS) andDr Michael Krings (Bavarian State Collection ofPalaeontology Munich, Germany) for their helpful commentsand insightful discussion. We thank William DiMichele andan anonymous reviewer whose critical and detailed commentsgreatly improved this paper. Financial support was partly pro-vided by the Chinese Academy of Science ProjectKZCX2-EW-120, National Basic Research Program of China(973 Program, 2012CB821901), the National Natural ScienceFoundation of China (to Z. Feng and J. Wang) and theVolkswagen Foundation (Az.: I/84638).

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Complete tylosis formation in a latest Permian conifer stem

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