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Morpho-Anatomical and Molecular Characterization of the Oversprouting Symptoms Caused by Fusarium decemcellulare in Guarana Plants (Paullinia cupana var. sorbilis)

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Abstract

Oversprouting is a poorly studied disease of guarana plant (Paullinia cupana var. sorbilis), a native species from Amazon Rainforest caused by Fusarium decemcellulare (FDC) that affects the plant growth and reproduction, severely compromising productivity. The sorbilis variety of guarana is anciently cultivated and is used today for the industry of soft drinks, cosmetic and pharmaceutical. Transcriptome, proteome, light and electron microscopy were used to compare symptomatic and asymptomatic tissues and reveal anatomical, histological and cytological alterations resultant from the disease. Disease symptoms described here include a marked reduction in the longitudinal axis and the formation of “capsules”, named as this for the first time here, which display hard thickened external walls and contain extremely malformed floral organs and/or poorly differentiated vegetative primordia when occurring isolate in individual branching points. The aggregate of multiple “capsules” in a same branch point produces galls. The production of indol-acetic acid (IAA) in vitro by F. decemcellulare was for the first time reported and the comparative transcriptome and preliminary proteome data from symptomatic and asymptomatic tissues, support the occurrence of hormonal imbalance identified through several plant hormone-related genes and proteins differentially expressed only in symptomatic tissues. Auxin signaling mechanism, as well as auxin-responsive genes associated to cell cycling, division and proliferation also occurred differentially in infected tissues. Oversprouting and the reduction of the longitudinal axis in malformed cells and organs are related to hormonal unbalance are discussed in this paper.

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Acknowledgments

The authors thank Sérgio de Araújo Silva of the Plant Physiology Laboratory for their technical support. We acknowledge to Dr. Adriana Franco Paes Leme and Dr. Bianca Alves Pauletti from Brazilian Biosciences Laboratory (LNBio), CNPEM, Campinas, Brazil (Mass Spectrometry Laboratory), for the infrastructure provided and technical support; to collegeagues at colleagues at Embrapa Dr. Firmino José do Nascimento Filho, for his help in collecting plant material, to Karina Bichara for the photos provided, to Jeferson Chagas for the technical and laboratory support. Special thanks to Dr. Paula Cristina da Silva Ângelo for her help in the anatomical studies, dissection of reproductive and vegetative structures and collaborations in the writing of this paper. The first author thanks CAPES for the scholarship. The research was supported by the Amazonas State Research Foundation (FAPEAM), National Council for Scientific and Technological Development (CNPq) and this study was financed also in part by the Coordenação deAperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) -Finance Code 001 (88887.200468/2018-00) - PROCAD-Amazônia.

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Authors and Affiliations

  1. Universidade Federal do Amazonas, Manaus, 69080-900, Brazil

    Claudia Afras de Queiroz, Igor Kelvyn Cavalcante Lobo, Sandra Barbosa de Sousa, Edmar Vaz de Andrade & Isabelle Bezerra Cordeiro

  2. Universidade Federal de Roraima, Boa Vista, 69300-000, Brazil

    Kedma da Silva Matos

  3. Embrapa Agroindústria Tropical, Fortaleza, 60511-110, Brazil

    Celli Rodrigues Muniz & Guilherme Julião Zocolo

  4. Embrapa Informática Agropecuária, Campinas, 13083-970, Brazil

    Michel E. Beleza Yamagishi

  5. Instituto Nacional de pesquisa da Amazônia, Manaus, 69060-001, Brazil

    Rogério Eiji Hanada

  6. Embrapa Amazônia Ocidental, Laboratório de Biologia Molecular, Rodovia AM-010, Km 29 - 69010-970, Manaus, Amazonas, Brazil

    Luadir Gasparotto, Anderson Adriano Martins Melo & Gilvan Ferreira da Silva

  7. Embrapa Cocais, São Luís, Maranhão, 65065-470, Brazil

    Nelcimar Reis Sousa

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Fig S1

Vegetative buds in asymptomatic branches and branches with symptoms of oversprouting in guarana plants. A: asymptomatic axillary vegetative bud in differentiation, with the longitudinal axis longer than the transversal. B: symptomatic vegetative bud, showing shortening of the longitudinal axis and increase of the transversal axis, with bracts organised concentrically on the same longitudinal plane. C: cross section of a branching point in an asymptomatic plant with very young secondary branch (Acosta et al. 2013) and axillary buds protected by foliaceous bracts (Andrews 2010). D: cross section of a “capsule” excised from a symptomatic branch. Malformed meristems or meristematic cores are encapsulated by the very thick outer layer (yellow circle). E: transection of a symptomatic branching point exactly in the plane of connection of a “capsule”. At least two meristematic cores can be supposed to exist inside the “capsule” delimited by a thick outer layer, and one of those (Acosta et al. 2013) could probably differentiate in a secondary branch in an asymptomatic node. F and I: longitudinal sections of “capsules” from symptomatic branches. In I the deeper staining with toluidine blue indicates what would be rows of small new formed or meristematic cells, composing at least three active cores inside the same “capsule” delimited by extremely thick wall (red arrows), which is composed by a set of imbricated thickened pieces that would be malformed bracts. G: asymptomatic young branch, in cross section. H: young branch in symptomatic plant, with thickening of the cortex. J-K: apical portions of guarana plant branches. The white bars indicate the planes of the transversal sections to show the internal structures in the details on the right side of the figure. Asterisks indicate the surfaces of the main branches. J: asymptomatic guarana plant presenting secondary branches originated from differentiation and elongation of axillary buds in four nodes and the initial signs of differentiation in the most apical bud. K: symptomatic guarana plant, displaying “capsules” in five branching nodes replacing secondary branches that should have differentiated and reduced internodes. (Scale bars A-H = 2 mm, J and K = main Fig. 1 cm and details 5 mm; I = 800 μm). (PNG 2634 kb)

High resolution image (TIF 5762 kb)

Fig. S2

Galls in the main branch of adult guarana plants show proliferation of “capsules” from vegetative buds (A-D). E-H: “Capsules” bunch in the branching node of nursery young plant, during the initial formation of galls. E: at least nine “capsules” can be counted on one branching point. F: longitudinal section of the structure in E, showing approximately five “capsules” and a basal connector tissue (BC), which makes the connection between the “capsules” themselves and to the plant branch, forming the gall. G: less affected branch of a nursery young plant with at least four “capsules” juxtaposed consecutively and not side by side. H: longitudinal section of the structure in G showing the basal connector tissue. I-L: Oversprouting symptoms in nursery young plant branch. I: “capsule” seen externally, red line indicates the plane of the cross section shown in K. The proliferation of trichomes in the outer surface of the “capsule”, a characteristic of protection bracts overexpressed in symptomatic tissues, is easily perceived. J: the same “capsule”, as in I viewed from above to show the thickness of the surrounding outer layer and the presence of poorly differentiated and malformed organs inside L: histological cut of the same “capsule”, stained with toluidine blue. (*) Air-space inside the “capsule”. Red arrows indicate the outer layer of the “capsules”, which are likely to be extremely thickened bracts. Circles indicate possible independent and malformed meristems. (Scale bars B and D = 5 mm; E-K = 5 mm; L = 800 μm). (PNG 3216 kb)

High resolution image (TIF 6093 kb)

Fig. S3

GO terms (top 50) associated to differentially expressed genes (Cellular Component). (PNG 25 kb)

Fig. S4

GO terms (top 50) associated to differentially expressed genes (Biological Process). (PNG 24 kb)

Fig. S5

GO terms (top 50) associated to differentially expressed genes (Molecular Function). (PNG 19 kb)

Fig. S6

Detection of Indole-3-Acetic Acid (IAA) by UPLC- QTOF-MSE. A) Chromatogram in negative-ion mode Full Scan (m/z 120–1180 Da). B) Extracted ion (m/z 174.05). The retention times of the compound are: (A) 5.29 min for analytical standard (IAA from plant origin) and 5.34 min for Fusarium decemcellulare (CML 3423). (B) 5.30 min for analytical standard and F. decemcellulare (CML 3423). (PNG 584 kb)

High resolution image (TIF 5409 kb)

Fig. S7

Mass spectra data for the molecule of Indole-3-Acetic Acid (IAA) precursor (m/z 174.05) and product (m/z 130) for analytical standard, from plant origin, and Fusarium decemcellulare CML 3423) analysed in the negative-ion mode. (PNG 724 kb)

High resolution image (TIF 6283 kb)

Fig. S8

Guarana plant oversprouting complex. A- Hyperplasia and hypertrophy of inflorescences; B- Hyperplasia and hypertrophy of the vegetative bud; C – Galls of “capsules” from reproductive tissue (galls with flower aspect); D - Galls of “capsules” from vegetative buds. (JPG 1855 kb)

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de Queiroz, C.A., da Silva Matos, K., Lobo, I.K.C. et al. Morpho-Anatomical and Molecular Characterization of the Oversprouting Symptoms Caused by Fusarium decemcellulare in Guarana Plants (Paullinia cupana var. sorbilis). Tropical Plant Biol. 13, 274–286 (2020). https://doi.org/10.1007/s12042-020-09256-1

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