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Characterization of Leaf Starch from HLB-Affected and Unaffected-Girdled Citrus Trees

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Characterization of Leaf Starch from HLB-Affected and Unaffected-Girdled Citrus Trees Physiological and Molecular Plant Pathology 79 (2012) 71e78 Contents lists available at SciVerse ScienceDirect Physiological and Molecular Plant Pathology journal homepage: www.elsevier.com/locate/pmpp Characterization of leaf starch from HLB-affected and unaffected-girdled citrus trees Pedro Gonzalez a, Jose Reyes-De-Corcuera b, Ed Etxeberria a,* a Department of Horticultural Sciences, University of Florida/IFAS, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, Florida 33850, USA b Department of Food Science and Human Nutrition, University of Florida/IFAS, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, Florida 33850, USA article info abstract Article history: Starch content in leaves of HLB (Huanglongbing or citrus greening)-affected branches increases sharply Accepted 21 May 2012 compared to those from non-HLB trees. Starch not only over-accumulates in photosynthetic cells, but starch grains become prominent in vascular parenchyma and sieve elements as well. These observations Keywords: imply strong disturbances in starch metabolism and photoassimilate partitioning in HLB-affected trees. Citrus greening Based on the elevated starch content, appearance of starch granules in phloem elements, and previous Candidatus Liberibacter asiaticus reports of the pathogen effect on starch properties, we hypothesized that starch from HLB-affected citrus Starch properties trees may differ morphologically, physically and/or chemically from starch accumulated in otherwise healthy leaves. To obtain starch granules from healthy trees of comparable size to those of HLB-affected trees, we girdled 2-year-old branches and allowed starch to accumulate for 3 months. Starch morphology was investigated under brightfield, polarized light and SEM. HLB-induced starch grains were not morphologically different in size, shape and overall appearance from those of girdled branches. When reacted with 2% I2, no significant difference was observed in the absorption spectra of whole starch fractions (lmax for HLB ¼ 604.1 and girdled 606.2 nm, respectively; n ¼ 6; p 0.05) nor in their amylose/ amylopectin ratio (HLB ¼ 1.4 Æ 0.17 and girdled ¼ 1.16 Æ 0.07, p 0.05) after chromatographic sepa- ration. However, lmax for individual fractions of HLB-affected leaves increased between 11 and 14 nm indicating a significant increase in the degree of polymerization of chain lengths of 12e45 glucose units. The increase in amylopectin chain length was confirmed by the rise in gelatinization temperature of approximately 10 C observed by polarized light microscopy. Our results indicate that starch grains from leaves affected by HLB were morphologically similar but differed biochemically from those formed by healthy trees after phloem blockage caused by mechanical injury. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction spread has brought renewed interest on this disease given its devastating potential to the world’s citrus industry. Citrus huanglongbing (HLB or citrus greening) is a highly In citrus trees, specific HLB symptoms do not exist. Some destructive, fast spreading disease of citrus. The disease is associ- symptoms such as yellow shoots, leaf blotchy mottle, and lopsided ated with a fastidious, Gram-negative, obligate parasite, phloem- fruits with color inversion and aborted seeds are characteristic, but limited a-protobacterium (Candidatus Liberibacter) [15,22] not yet they do not always occur together in the same tree, they can be fully cultured, although recent attempts have resulted in limited distorted or masked by symptoms of other diseases, or induced by success [10,32]. Long established in eastern Asia and South Africa conditions other than HLB [6]. Amongst other HLB-induced char- [6,9], the disease is now well established in Brazil [7,38], and the acteristics, Schneider [30] noted massive starch build-up in leaves states of Florida [5,18], Louisiana and in Puerto Rico [11]. Its rapid and petioles which otherwise accumulate little or no starch under normal conditions [43]. Detectable amounts of foliar starch are only sporadically observed as a result of zinc deficiency [33] or girdling (as in severed branches). Schneider [30] concluded that starch l Abbreviations: HLB, huanglongbing or citrus greening; max, wavelength of accumulation resulted from the obstruction of photoassimilate maximum absorbance; MES, 4-Morpholineethanesulfonic acid; PCR, Polymerase transport by necrotic phloem pockets scattered throughout the Chain Reaction; SEM, Scanning Electron Microscope. * Corresponding author. Tel.: þ1 863 956 1151. foliar vascular system prompting accelerated rates of starch E-mail address: eetxeber@ufl.edu (E. Etxeberria). synthesis in leaves. In fact, the yellowing leaf mottle symptoms of 0885-5765/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.pmpp.2012.05.002 72 P. Gonzalez et al. / Physiological and Molecular Plant Pathology 79 (2012) 71e78 HLB-affected leaves are believed to result from the disintegration of months of girdling, with leaf abscission becoming prominent after the chloroplast thylakoid system caused by the bulky starch build- 6 months. This ensured that starch granules had reached their up. Similar leaf yellowing as a result of thylakoid damage from maximum size becoming comparable to those from HLB-affected starch accumulation can be artificially induced by branch girdling leaves, thus eliminating any possible effect due to size. of citrus trees [31]. In most instances, leaves from girdled branches For comparative purposes, commercial starch samples from rice, display characteristics that closely resemble those from HLB- wheat and potato were used. These were all purchased from Sigma, affected trees. St. Louis, MO (rice, S-7260; wheat, S-5127; potato, S-2004). Recently, Etxeberria et al. [12] and Folimonova et al. [13] reported that starch grains, besides accumulating in virtually 2.2. Starch extraction and isolation every photosynthetic and parenchyma cell of all aerial parts [12], are also found in phloem sieve elements [13], a rare condition in For the isolation of starch granules from leaf tissue, three tissue higher plants. The profound changes in starch content were later discs from a single leaf, made with a paper hole puncher verified by studies using Fourier transform infrared-attenuated (27.3 mm2), were homogenized in 2-mL capped tubes containing total reflection spectroscopy [20] where divergences in the 500 mL of water and four metal beads (2.36 mm diameter) (Mobio regions attributable to carbohydrate vibrational bands indicated Laboratories, California). Homogenization was carried out in two chemical alterations (amount, type or structure) to the carbohy- 40-s cycles for a total of 80 s using a Precellys 24 Tissue Homoge- drate fractions. In support of the observed starch increases, Kim nizer (Bertin Technologies, France). The homogenate was subse- et al. [23] reported up-regulation of starch biosynthetic enzymes in quently placed on top of a 50% sucrose cushion and starch granules HLB-affected leaves. precipitated at 1 g. The pellet containing starch granules was Starch is a natural product of photosynthetic CO2 fixation in washed three times with water in conical microfuge tubes and green tissues. Formed by a-1,4 glucose linkages, starch exists in two centrifugation at 10 Â g. The final pellet was dried overnight under forms, the soluble, small linear chain amylose and the highly vacuum in a desiccator containing calcium sulfate. Starch samples branched insoluble amylopectin [42]. In plants, starch is composed were stored at room temperature in a separate desiccator until use. mainly of 30% amylose and 70% amylopectin [34], with specific ratios varying amongst species. It is also well established that the 2.3. Grain morphology levels of plant starches [21,24] and their physical, biochemical and morphological characteristics are highly influenced by many Starch samples, re-suspended in water, were filtered under conditions ranging from environmental factors [35], genetic alter- vacuum using cellulose nitrate membrane filter papers (0.2 mm ations [8,16] and pathogen infection [19,27,29,36,37]. Whatman GmbH) and dried overnight in a vacuum desiccator. The Leaves from accidentally severed (girdled) branches are often dried starch was mounted on stubs and coated with gold/palladium symptomatically indistinguishable from HLB-affected citrus leaves, using a Ladd sputter coater (Ladd Research Industries, Burlington, including the accumulation of high levels of starch. Based on the VT). Samples were viewed using a Hitachi S530 SEM (Tokyo, Japan) unusual tissue distribution [12], appearance of starch granules in and photographed using a Canon EOS Rebel XT digital camera phloem elements [13], and previous reports of pathogen effect on (Tokyo, Japan). plant starch properties [8,19,29,36,37], it is reasonable to expect that starch from HLB-affected citrus trees will differ in morphology, 2.4. Gelatinization physical and/or chemical properties from starch accumulated under the absence of pathological conditions. Starch gelatinization was characterized by controlled tempera- To further understand the physiological and metabolic effects of ture polarized light microscopy. Starch granules were re-suspended HLB on citrus trees, we initiated the present study aimed at char- in 50% glycerol due to a high mobility of starch granules in water acterizing selected properties of starch grains from HLB-affected alone. Polarized light microscopy was performed using
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