Mechanical stress caused by wind on leaves of Theobroma cacao: Photosynthetic, molecular, antioxidative and ultrastructural responses

PLoS One. 2018 Jun 27;13(6):e0198274. doi: 10.1371/journal.pone.0198274. eCollection 2018.

Abstract

Theobroma cacao is cultivated in the shade, in a so-called 'Cabruca' system, in intercropped with Erithryna or other tree species of economic value, and in full sun as a monoculture in irrigated or chemically-irrigated systems. Since it is a species quite intolerant to wind, it is practically impossible to implant cacao crops under full exposure to the sun, or in areas of frequent winds, without the protection of windbreaks, using arboreal species around the area of culture in the form of box. Wind can cause mechanical stimuli in plants, affecting their growth and development. The objective of this work was to evaluate the photosynthetic changes in mature leaves and the molecular, biochemical and ultrastructural changes in young and mature leaves of the CCN 51 cloned genotype of T. cacao subjected to intermittent (IW) and constant (CW) wind, with velocities of 2.5, 3.5 and 4.5 m s-1, during 3, 6 and 12 h of exposure. It was verified that CW and IW, considering different exposure times, interfered directly in stomatal conductance (gs), transpiration (E) and water use efficiency (WUE), causing a reduction of the photosynthetic rate (A) in mature leaves. In addition, the pulvinus and blade of young and mature leaves, exposed to IW and CW with different exposure times (3 and 12 h), showed marked macroscopic and microscopic mechanical injuries resulting from the constant leaf movement. At both speeds, there was rupture of the cell nuclear membrane in pulvinus and the mesophyll tissues, mainly in the young leaves. On the other hand, in young and mature leaves exposed to CW and IW at different speeds and exposure times, there was lipid peroxidation, increased activity of guaiacol (GPX) and ascorbate (APX) peroxidases in most treatments; and altered expression of transcripts of psba and psbo genes related to the phothosynthetic apparatus and Cu-Zn-sod and per genes related to antioxidative enzymes at the rate of 4.5 m s-1. Younger leaves were more intolerant to mechanical stress caused by the wind, since presented greater macro and microscopic damages and, consequently, greater molecular, biochemical and ultrastructural changes. High wind speeds can seriously compromise the development of young leaves of T. cacao plants and affect their productivity.

MeSH terms

  • Ascorbate Peroxidases / metabolism*
  • Cacao / growth & development*
  • Cacao / ultrastructure
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Plant
  • Genotype
  • Lipid Peroxidation
  • Nuclear Envelope / ultrastructure
  • Peroxidase / metabolism*
  • Photosynthesis
  • Plant Leaves / growth & development
  • Plant Leaves / ultrastructure
  • Plant Proteins / metabolism
  • Stress, Mechanical*
  • Wind

Substances

  • Plant Proteins
  • guaiacol peroxidase
  • Ascorbate Peroxidases
  • Peroxidase

Grants and funding

The authors received no specific funding for this work.