Morphological Characterization of Prickled and Prickle-Free Rubus

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Morphological Characterization of Prickled and Prickle-Free Rubus HORTSCIENCE 55(5):676–683. 2020. https://doi.org/10.21273/HORTSCI14815-20 growths, but for clarity and as correct botanic terminology, the term prickle for the presence of epidermal appendages and Morphological Characterization of prickle-free for the absence is used in this manuscript. Prickled and Prickle-free Rubus Using The genus Rubus is an excellent member of the family Rosaceae to understand prickle Scanning Electron Microscopy initiation and development. Fruits of the genus Rubus, also known as caneberries or Archana Khadgi and Courtney A. Weber brambles, are an important source of cellu- School of Integrative Plant Science-Horticulture Section, Cornell University, lose, vitamin E, natural pigments, antioxi- Cornell AgriTech, 630 W. North Street, Geneva, NY 14456 dants, and phenolic compounds (Beattie et al., 2005). Prickles are an unappealing trait Additional index words. blackberry, black raspberry, glandular trichome, prickle, raspberry, in red and black raspberry and blackberry simple trichome (Clark et al., 2007), as well as in many wild Rubus species. Prickles complicate both fruit Abstract . Caneberry crops (raspberry and blackberry) are globally commercialized harvesting and field management (pruning, specialty crops with a high fresh market value. Field management of canes and training). Because of this, there have been harvesting of fruits can be complicated by the presence of prickles (the botanically many efforts to use the prickle-free pheno- accurate term rather than spines or thorns) on the stems, petioles, and underside of the type in breeding, thus resulting in the prickle- leaves. Both field management and fruit harvesting could be simplified by the develop- free cultivars such as ‘Joan J’ and ‘Glen ment of cultivars with prickle-free canes. Scanning electron microscopy (SEM) was used Ample’ red raspberry (R. idaeus L.) (Finn Rubus to analyze and compare prickle development in different species. Comparisons et al., 2008), and ‘Natchez’, ‘Chester’ (Clark Rubus idaeus were made between prickled vs. prickle-free red raspberry ( L.), black and Moore, 2008), ‘Apache’, and ‘Triple Rubus occidentalis Rubus raspberry ( L.), blackberry ( hybrid), complex hybrid with Crown’ blackberry (R. hybrid), among R. occidentalis 3 R. idaeus (Rubus purple fruit ( ), and the hairy and prickled wineberry others. The prickle-free phenotype has long phoenicolasius Maxim). Samples from stems and leaves with petioles attached were used been sought after in blackberry sports of for imaging. There were distinct differences between prickled vs. prickle-free phenotypes popular cultivars; however, combining the in each species. The images of prickle development suggest that prickles either develop prickle-free trait with other important traits directly from glandular trichomes (in red raspberry and wineberry) or that the signal through traditional breeding approaches can originates from glandular trichomes (in blackberry). Black raspberry prickle develop- be time-consuming and difficult because of ment was similar to that of blackberry, suggesting that prickles developed after a polyploidy and/or high heterozygosity among developmental signal from glandular trichomes rather than as a direct development the germplasm. Because the genus has both from glandular trichomes. The prickle development in the purple hybrid was unique in prickled and prickle-free cultivars with the presence of one-sided lumps in the trichomes, which has not been seen in any other similar genetics, comparisons at both the Rubus species to date; however, both prickled and prickle-free plants exhibited simple morphological and molecular levels is pos- nonglandular trichomes. Unlike previous studies, an increase in the number of simple sible in understanding prickle development. trichomes was not specific to prickle-free plants, but rather variability among the This knowledge is the first step toward the different genotypes was observed. This study adds to the basic understanding of prickle development of prickle-free versions of Rubus development in the genus as a first step in the development of prickle-free versions economically important cultivars using of important cultivars through gene-editing procedures for improving the ease of field genome-editing techniques. management and harvesting. An analysis (Coyner et al., 2005) of prickle development using a blackberry prickle chimera provided a significant step Plant trichomes are simple hair-like struc- et al., 2004). In Arabidopsis (Arabidopsis in understanding how different embryonic tures that extend from the epidermal surface thaliana), unicellular simple trichomes have layers (LI,LII,LIII) communicate for prickle of plants and are present on most terrestrial proven to be great models for understanding formation. In the study, the chimeric black- plants (Johnson, 1975). Trichomes increase cell fate and differentiation (Breuer et al., berry, which produced prickles in only a few the ability of the epidermal layer to moderate 2009; Marks et al., 2009; Wagner, 1991). regions of the plant, was characterized. The surface temperatures and reduce transpiration Glandular or secreting trichomes are present results provided evidence of communication as the pubescence traps air, which effectively in many vascular plants and are multicellular between epidermal and cortical cells for thickens the barrier between the epidermis structures with secreting glands at the tip of prickle development in blackberry. On the and the environment (Schuepp, 1993). In the stalk, which often produce and store removal of outermost layer (LI-derived epi- addition to abiotic stresses, trichomes are terpenoids, phenylpropanoid oils, and other dermal layer) of the prickle-free area, known to protect plants against herbivores, secondary metabolites (Mahmoud and Cro- prickles were produced from the layer under- insects, pathogens, and mechanical injuries teau, 2002; Schilmiller et al., 2008; Wagner neath (LII-derived cambial layer), suggesting (Barton, 2014; Halpern et al., 2007; Szyman- et al., 2004). Other epidermal outgrowths the presence of molecular cues between the ski et al., 2000). Trichomes vary greatly in include thorns, prickles, and spines. Al- two layers. There have been additional stud- their morphology, but can be classified into though these terms refer to botanically dif- ies in understanding morphological struc- two types: simple trichomes (nonsecreting) ferent structures with different features, all tures, histochemical features, origin, and and glandular (secreting) trichomes (Wagner are commonly referred to as ‘‘thorns’’; how- genetic patterns of prickles in Rosaceous ever, botanically, thorns are modified branches species (Asano et al., 2008; Kellogg et al., and spines are modified leaves, both contain- 2011; Rajapakse et al., 2001). Although ing adjoining vascular tissue. In contrast, prickles of red raspberry consist of only Received for publication 10 Jan. 2020. Accepted prickles are formed by multiple cellular divi- epidermal tissues, prickles of blackberry for publication 27 Feb. 2020. sions of the epidermis and do not contain comprise both epidermal and cortical tissues Published online 6 April 2020. C.A.W. is the corresponding author. E-mail: caw34@ internal vascular tissue (Bieniek and Millington, but still lack vasculature (Kellogg, 2009). cornell.edu. 1967; Blaser, 1956; Coyner et al., 2005; There is limited knowledge regarding the mo- This is an open access article distributed under the Esau, 1977; Posluszny and Fisher, 2000). lecular pathways contributing to the prickle- CC BY-NC-ND license (https://creativecommons. Most bramble research uses the term thorns free trait, which has hindered the application org/licenses/by-nc-nd/4.0/). to refer to these multicellular epidermal out- of modern molecular approaches to studying 676 HORTSCIENCE VOL. 55(5) MAY 2020 prickle development. To identify the mo- was made between ‘Joan J’ and ‘Caroline’ to osmium tetroxide (OsO4) for 2 h. The sam- lecular pathways controlling prickle devel- obtain a population segregating for prickles. ples were subsequently dehydrated through a opment, a thorough understanding of prickle Seeds from this cross were collected, steril- series of ethanol soaks of 25% (10 min), 50% morphology in the genus is required to ized, and cultured in media for germination in (10 min), 70% (overnight), 95% (10 min), serve as the foundation for these additional a growth chamber. After germination, the and 100% (overnight). The samples were studies. seedlings were transferred to soil and grown then critical point dried using dry carbon A previous morphological study on un- in a growth chamber before transfer to a dioxide with exchange conditions of 10 °Cat derstanding prickle development in Rubus greenhouse. The population segregated al- 3.4 atm (1 atm = 101.325 kPa) and then at suggested that prickles are modified glandu- most perfectly 1:1 for the absence/presence 31 °C at 4.76 atm. The dried samples were lar trichomes (Kellogg et al., 2011). In the of prickles. Images from all the individuals, sputter coated with gold (Desk IV cold study, the prickled red raspberry cultivar including segregating progeny from the ‘Joan sputter coater; Denton Vacuum, Moores- Heritage and the low prickle cultivar Canby, J’ · ‘Caroline’ population, were examined town,NJ)andviewedusinganAspexPICA the prickle-free blackberry cultivar Arapaho using a scanning electron microscope. 1020 scanning electron microscope (Aspex, and the fully prickled cultivar Prime Jim, and Microscopy. SEM
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