The Sisal Virome: Uncovering the Viral Diversity of Agave Varieties Reveals New and Organ-Specific Viruses.

Gabriel Quintanilha-Peixoto,Marcelo Falsarella Carazzolle,Ana Cristina Fermino Soares,Dener Eduardo Bortolini,Piotr Mieczkowski,Eric Roberto Guimarães Rocha Aguiar,Marina Pupke Marone,Gonçalo Amarante Guimarães Pereira,Fábio Trigo Raya,Aristóteles Góes-Neto,Christian A Voigt,Roenick Proveti Olmo,Paula Luize Camargos Fonseca

doi:10.3390/microorganisms9081704

Abstract

Sisal is a common name for different plant varieties in the genus Agave (especially Agave sisalana) used for high-quality natural leaf fiber extraction. Despite the economic value of these plants, we still lack information about the diversity of viruses (virome) in non-tequilana species from the genus Agave. In this work, by associating RNA and DNA deep sequencing we were able to identify 25 putative viral species infecting A. sisalana, A. fourcroydes, and Agave hybrid 11648, including one strain of Cowpea Mild Mottle Virus (CPMMV) and 24 elements likely representing new viruses. Phylogenetic analysis indicated they belong to at least six viral families: Alphaflexiviridae, Betaflexiviridae, Botourmiaviridae, Closteroviridae, Partitiviridae, Virgaviridae, and three distinct unclassified groups. We observed higher viral taxa richness in roots when compared to leaves and stems. Furthermore, leaves and stems are very similar diversity-wise, with a lower number of taxa and dominance of a single viral species. Finally, approximately 50% of the identified viruses were found in all Agave organs investigated, which suggests that they likely produce a systemic infection. This is the first metatranscriptomics study focused on viral identification in species from the genus Agave. Despite having analyzed symptomless individuals, we identified several viruses supposedly infecting Agave species, including organ-specific and systemic species. Surprisingly, some of these putative viruses are probably infecting microorganisms composing the plant microbiota. Altogether, our results reinforce the importance of unbiased strategies for the identification and monitoring of viruses in plant species, including those with asymptomatic phenotypes.

Highlights

Sisal is a common name for different species and hybrid varieties in the genus Agave cultivated worldwide for the production of hard natural fibers [1,2]
A. fourcroydes displayed the highest diversity among the three Agave taxa while the roots were the plant organ with the highest viral diversity
~0.02% of all transcripts assembled for almost all the organs and varieties, with exception of the roots of Agave fourcroydes (0.04%) and Agave Hybrid 11648 (0.03%) and the leaves of

Summary

Introduction

Sisal is a common name for different species and hybrid varieties in the genus Agave (especially Agave sisalana) cultivated worldwide for the production of hard natural fibers [1,2]. The cultivated Agave species are not native to that region, they are adapted to the specific environmental conditions of this area, including low rainfall, high temperatures, and low aboveground biomass coverage [7]. These traits of resistance to abiotic stresses make sisal one of the few cultivation options available in the Caatinga biome, historically neglected in infrastructure projects. Viral infections in plants may cause damage to specific structures, such as the photosynthetic apparatus in the leaves [8], the roots system [9], and in growth and development, as in early flowering, often used to accelerate yielding [10] In sisal, these forms of damage could harm fiber quality, which is the main commercial and valuable trait in these

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