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An Anatomical Study of Developmental Changes in Maturing Root Tissues of Pomegranate (Punica Granatum L.) and Formation of a Unique Type of Periderm

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An Anatomical Study of Developmental Changes in Maturing Root Tissues of Pomegranate (Punica Granatum L.) and Formation of a Unique Type of Periderm www.plantroot.org 33 Original research article An anatomical study of developmental changes in maturing root tissues of pomegranate (Punica granatum L.) and formation of a unique type of periderm Astha Tuladhar and Naosuke Nii Faculty of Agriculture, Meijo University, Nagoya 468-8502, Japan Corresponding author: N. Nii, E-mail: [email protected], Phone: +81-52-838-2435 Received on March 24, 2014; Accepted on July 10, 2014 Abstract: Roots of pomegranate (Punica underway to acknowledge changes in such granatum L.), belonging to Punicaceae, were biopolymer accumulation in the outermost tissue investigated anatomically to record changes in in abiotic stress conditions. tissue development from growth to maturity. When roots start secondary growth, a protective Keywords: lignin, suberin, rhizodermis, exodermis, tissue called polyderm composed of alternating thick-walled cells, polyderm, Punicaceae suberized and non-suberized cell layers, develop beyond the endodermis in certain families of Introduction plants including Myrtaceae. Punicaceae family is not known to develop a polyderm. However, new Pomegranate (Punica granatum L.) belongs to layers formed beyond the endodermis during Punicaceae family of plants. It is an oldest known secondary growth and biopolymer deposition edible fruit tree species originating from central Asia was observed in their cell walls. The present which is now produced worldwide for its highly study aims to gather more knowledge on this recognized medicinal, nutritional and ornamental tissue discovered in pomegranate roots and properties (Teixeira da Silva et al. 2013). Its adaptive cross check whether it is a polyderm or a unique characteristics reflect in its geographically wide type of periderm. distribution. Roots are directly affected by different Root specimens were sectioned freehand or soil environments. Maintaining a healthy root system with an ultramicrotome after embedding in is crucial for a steady yearly production, especially in Technovit 7100 resin. After staining with the case of deciduous fruit trees such as pomegran- berberine hemisulfate-aniline blue-safranin O, ates that relies on starch deposited in roots over the root sections were observed under winter. Unfortunately, there is very limited data on fluorescent or optical microscopes. pomegranate roots. A study on pomegranate root Unlike the polyderm in Myrtaceae roots, in distribution was reported recently by Hiwale et al. pomegranate roots, ligno-suberic material (2011) but an anatomical study like the present study accumulated in every cell layer beyond the is still rare. One reason could be because pomegran- endodermis. The alternating suberized and ates are known to have toxic bark and roots (Tripathi non-suberized layers that define the polyderm and Singh 2000). were absent. Lignin accumulation in the cell wall In this study, pomegranate roots were investigated was pronounced in every cell layer of this anatomically to gain basic knowledge of root tissue outermost tissue and suberin-like development from growth to maturity. Recording autofluorescence was also observed in the same changes that occur during root growth may further layer. We considered this to be a unique feature clarify tissue function and point out interesting typical in pomegranate periderm. characteristics unique to pomegranate roots. In the It is possible that accumulating both lignin and past, we have reported similar works in grapevine suberin in the same cell layer instead of roots (Song et al. 2011b) with special focus on the alternative layers is more efficient because Casparian strip. In the present study, our focus is metabolic energy is not spent in forming a mainly on biopolymer accumulation during periderm separate cell layer. Further experiments are formation. _____________________________________________________________________________________________________________________________________________________________________________ Tuladhar A, Nii N 2014 An anatomical study of developmental changes in maturing root tissues of pomegranate (Punica granatum L.) and formation of a unique type of periderm. Plant Root 8: 33-41. doi:10.3117/plantroot.8.33 Copyrights 2014, Plant Root (JSRR), www.plantroot.org www.plantroot.org 34 Early observations on polyderm were reported by In this preliminary study, pomegranate roots Luhan (1955) in Unserer Alpenpflanzen and by grown in normal condition were continuously Nelson and Wilhelm (1957) and Mann (1930) in sectioned from the root tip to basal area to examine strawberry roots. Esau (1970) described polyderm as 1) the accumulation of lingo-suberic material in root a protective tissue composed of alternating suberized tissues such as rhizodermis/epidermis (ep), exo- and non-suberized cell layers. According to Esau dermis (ex), cortex (co), and endodermis (en) and 2) (1970) polyderm is found in only a few plant families the periderm formation process during secondary such as Myrtaceae, Hypericaceae, Onagraceae and growth. The results obtained from this observation Rosaceae families but Punicaceae was not mentioned. are intended to be used for further stress-response Recently, we studied the roots of feijoa (Feijoa related experiments. Compared to the polyderm sellowiana) belonging to Myrtaceae and reconfirmed found in Myrtaceae, in pomegranate roots, the the features of the polyderm development (Nii et al. alternating layers of suberized and non-suberized 2012). Based on our observations, polyderm in feijoa layers described as polyderm did not occur. Instead a roots formed due to the division of a single-layered cell layers with heavy lignin-like accumulation was pericycle into three layers at a time. Lignin accumu- observed in the outermost cell layers. In the recent lated in the outermost layer, immediately beyond the years, root biology is steadily gaining attention. In endodermis, and we called that layer thick-walled such a context, the present study about biopolymer cell layer (twc). Suberin accumulated in the middle accumulation in protective root tissues of woody layer forming the Casparian strip, so we called that roots during its maturing phases is highly appropriate layer endodermis-like cell layer (el). The innermost to broaden our knowledge about its function which layer retained the pericyclic characters, and it divided still needs much clarification. further to form a new set of three layers. During this observation, our attention was drawn to the accumu- Materials and Methods lation pattern of lingo-suberic materials. At the polyderm, biopolymers mainly lignin and suberin Approximately ten-year-old pomegranate trees (cv. accumulated on opposite sides of the cell wall in two ‘Wonderful’) which were propagated from cuttings separate cell layers. Lignin-like deposit was “closed” and grown under normal conditions in a greenhouse at centripetally resembling the letter “w” at the Meijo University were used for the present investiga- thick-walled cells whereas suberin-like deposit was tion. The pomegranate cuttings were grown in plastic “open” centripetally resembling the letter “m” at the pots (13 cm wide and 11 cm deep) filled with sandy endodermis-like cells and this accumulating pattern soil and watered when the upper surface of the soil was commonly detected in roots of five Myrtaceae became dry. The growth of pomegranate trees was species (unpublished data). dwarfed like bonsai by using small-sized plastic pots. For woody roots, accumulation of biopolymers Roots were collected from twenty different trees for such as lignin and suberin is of particular importance observation. To collect roots, plants were removed because it is known to protect plants from fungal from the pots and only roots with new white root tips diseases and insect attacks (Moerschbacher et al. were collected from the root tip to basal area. 1900, Nelson and Wilhelm 1957, Williamson 1984). Hand-sections of roots were prepared by using a The accumulation of biopolymers such as lignin and new stainless steel razor blade. Serial transverse suberin is a species-specific genetic feature and sections, commencing at approximately 5 mm from seems to be useful as a barometer to distinguish the root tip toward the basal portion of the root, were species. For example, phi-thickening is a kind of cut at 10 mm intervals to examine changes in struc- lignin accumulation found in Rosaceae species such tural development as roots matured. as apples (Mackenzie 1979) and loquats (Nii et al. Root specimens were examined under fluorescent 2004, Pan et al. 2006). In addition, our data shows microscopy (excitation wavelength 365 nm) with or that unfavorable growth conditions like flooding or without staining. Several different staining solutions, drought affects the accumulation of these biopoly- including berberine hemisulfate-aniline blue-safranin mers. Our studies revealed that under drought O were used (Brundrett et al. 1988). Lux et al. (2005) conditions, phi-thickenings developed markedly in reported a novel method for simultaneously clearing cortex cells of loquat trees (Nii et al. 2004, Pan et al. and staining tissues in which the fluorochrome 0.1% 2006). Similarly, in cortex of red bayberry roots, berberine hemisulfate was dissolved in a clearing crescent-shaped lignin accumulation increased under mixture consisting of pure lactic acid saturated with drought stress (Song et al. 2011a). Thus we felt the chloral hydrate. We used this method and incubated need to trace the biopolymer accumulation in root the root sections in 0.1% berberine hemisulfate
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