Functional Anatomy of the Oral Region of the Potato Psyllid (Hemiptera: Psylloidea: Triozidae)by Joseph M. Cicero, Philip A. Stansly, Judith K. Brown

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Functional Anatomy of the Oral Region of the Potato Psyllid (Hemiptera: Psylloidea: Triozidae)


Ann. Entomol. Soc. Am. 1?19 (2015); DOI: 10.1093/aesa/sav059

ABSTRACT ?Candidatus Liberibacter solanacearum?, causal agent of zebra chip of potato and veingreening of tomato, is prolific in tissues of the oral region of its vector, Bactericera cockerelli (Sulc). The region has, evolutionarily, reflexed under the head (?opisthognathy?), so that the mandibular stylets are ventral to the maxillary stylets, and both are directed posteriorly. The region includes the labium, furcasternum, and tentorium. The tentorium is a minute, crate-shaped, extremely complex endoskeletal apparatus consisting of preoral and postoral sections, with the primitive mouth in between. Except for certain prominent structures, its functional anatomy is poorly understood, and provisional (generic) terminology is needed to identify them. It is formed from several panel-shaped and rod-shaped invaginations of the preoral orifice. Panels divide the preoral section into four tissue blocks: hypopharynx, epipharynx, and two lateral blocks of questionable homological identity. Those between the hypopharynx and lateral blocks are fluted into ?holsters.? Holsters are extended into the postoral section as ?loading sleeves.? Together, both house the stylets. Stylet manipulation muscles are attached to them, not to the stylets themselves. Loading sleeves also function to guide presumptive stylets into their functional positions during a molt. Rods are located in the postoral section, and they form ?ecdysial gaps? which also assist in molting. Stylets converge toward the preoral orifice, designed to interlock the maxillars and redirect the mandibulars to their flanks to form a ?stylet bundle,? and rotate the bundle 90 so that it can curve, about its most-bendable axis, into a cuticular pouch or ?crumena? on exit.

KEY WORDS Liberibacter, oral region, stylet, tentorium, retortiform

The ?potato psyllid,? Bactericera cockerelli (Sulc) (Psylloidea: Triozidae) is considered to be the insect vector of the fastidious bacterium, ?Ca. Liberibacter solanacearum? (CLso; Hansen et al. 2008; Liefting et al. 2008, 2009) that is associated with zebra chip of potato (Munyaneza et al. 2007, Crosslin et al. 2010), and veingreening of tomato (Brown et al. 2010) diseases.

CLso has not yet been cultured, owing to its obligate nature. However, Ammar et al. (2011a, b) used highspecificity DNA probes and fluorescence in situ hybridization (FISH) to provide confirmatory evidence that the near-systemic bacteria in the Asian citrus psyllid,

Diaphorina citri Kuwayama, is in fact ?Ca. Liberibacter asiaticus? (CLas). J. M. C., T. W. Fisher and J. K. B. (unpublished data) used colloidal gold ISH to establish a morphotypic description of CLso which corresponds to, and therefore validates, bacteria referred to as CLso in potato psyllid-infested tomato (Liefting et al. 2009) and in Asian citrus psyllid-infested citrus phloem (Massonie et al. 1976, Bove 2006, Brlansky and Rogers 2007, Gottwald et al. 2007).

The present article is a morphological and functional elucidation of the oral region, launched with the discovery of morphotypic bacteria, profusely distributed in many tissues of this area that cannot be adequately identified. This elucidation will serve as the reference needed for a companion paper which details that distribution.

A comprehensive study of the literature revealed that prior works on the anatomy of the oral region are largely derived from the classical goal of associating internal and external cuticles with the primitive, orthopteroid condition, and developing a system of terminology that is based on the drawing of homologies (Snodgrass 1935,

Duporte 1962, Singh 1971). The complications created using the homological approach interfered with our goal to produce a functional interpretation of the oral region for broader audiences. Functional genomics databases (transcriptomes) and proteomic resources that can be used to develop corresponding molecular and cellular hypotheses toward identifying key psyllid?CLso/CLas effectors that mediate transmission processes necessarily require a commensurate understanding in functional anatomy that is accessible to nonphylogenetic, nonanatomical researchers.

Comparative, homological anatomy is a very important school of thought, but, with the exception of 1 School of Plant Sciences, University of Arizona, 303 Forbes Hall,

Tucson, AZ 85721. 2 Current address: Department of Entomology and Nematology,

University of Florida IFAS, Steinmetz Hall, 1881 Natural Area Dr.,

Gainesville, FL 32611. 3 Corresponding author, email: 4 University of Florida IFAS, Southwest Florida Research & Education Center, 2685 State Rd. 29 North, Immokalee, FL 34142.

VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America.

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Annals of the Entomological Society of America Advance Access published July 15, 2015 certain well-known, well-accepted terms, it will not be held in subscription here. Instead, a provisional set of terms that connote location and function will be used where needed. Lastly, in this article, the deprecated term ?homoptera? will be used throughout, as is relevant, to refer specifically to information published during the timeframe when homopterans were recognized as a separate Order.

Materials and Methods

Psyllid Colonies. Infected (CLso) adult potato psyllids were obtained from infested tomato plants in

Snowflake, AZ, during 2004, whereas uninfected (CLso?) adult potato psyllids were obtained that same year from greenhouse tomato plants in Willcox, AZ.

Additional CLso? colonies were obtained from potato fields in Hermiston, OR, and from the Yakima Agricultural Research Laboratory, Wapato, WA. Colonies were reared in separate insectaries on tomato plants placed in Bug Dorms (BioQuip Products, Rancho Dominguez,