Alternative oxidase capacity of mitochondria in microsporophylls may function in cycad thermogenesis

Yasuko Ito Inaba, Mayuko Sato, Mitsuhiko P. Sato, Yuya Kurayama, Haruna Yamamoto, Mizuki Ohata, Yoshitoshi Ogura, Tetsuya Hayashi, Kiminori Toyooka, Takehito Inaba

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Abstract

Cone thermogenesis is a widespread phenomenon in cycads and may function to promote volatile emissions that affect pollinator behavior. Given their large population size and intense and durable heat-producing effects, cycads are important organisms for comprehensive studies of plant thermogenesis. However, knowledge of mitochondrial morphology and function in cone thermogenesis is limited. Therefore, we investigated these mitochondrial properties in the thermogenic cycad species Cycas revoluta. Male cones generated heat even in cool weather conditions. Female cones produced heat, but to a lesser extent than male cones. Ultrastructural analyses of the two major tissues of male cones, microsporophylls and microsporangia, revealed the existence of a population of mitochondria with a distinct morphology in the microsporophylls. In these cells, we observed large mitochondria (cross-sectional area of 2 mm2 or more) with a uniform matrix density that occupied .10% of the total mitochondrial volume. Despite the size difference, many nonlarge mitochondria (cross-sectional area ,2 mm2) also exhibited a shape and a matrix density similar to those of large mitochondria. Alternative oxidase (AOX) capacity and expression levels in microsporophylls were much higher than those in microsporangia. The AOX genes expressed in male cones revealed two different AOX complementary DNA sequences: CrAOX1 and CrAOX2. The expression level of CrAOX1 mRNA in the microsporophylls was 100 times greater than that of CrAOX2 mRNA. Collectively, these results suggest that distinctive mitochondrial morphology and CrAOX1-mediated respiration in microsporophylls might play a role in cycad cone thermogenesis.

Original languageEnglish
Pages (from-to)743-756
Number of pages14
JournalPlant physiology
Volume180
Issue number2
DOIs
Publication statusPublished - Jun 2019

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All Science Journal Classification (ASJC) codes

  • Physiology
  • Genetics
  • Plant Science

Cite this

Inaba, Y. I., Sato, M., Sato, M. P., Kurayama, Y., Yamamoto, H., Ohata, M., ... Inaba, T. (2019). Alternative oxidase capacity of mitochondria in microsporophylls may function in cycad thermogenesis. Plant physiology, 180(2), 743-756. https://doi.org/10.1104/pp.19.00150