Gene expression and metabolite levels converge in the thermogenic spadix of skunk cabbage

Haruka Tanimoto; Yui Umekawa; Hideyuki Takahashi; Kota Goto; Kikukatsu Ito

doi:10.1093/plphys/kiae059

Gene expression and metabolite levels converge in the thermogenic spadix of skunk cabbage

Plant Physiol. 2024 Feb 6:kiae059. doi: 10.1093/plphys/kiae059. Online ahead of print.

Authors

Haruka Tanimoto¹, Yui Umekawa², Hideyuki Takahashi³, Kota Goto⁴, Kikukatsu Ito^{1

4}

Affiliations

¹ United Graduate School of Agricultural Science, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan.
² Akita Research Institute of Food and Brewing, 4-26 Sanuki, Araya-machi, Akita 010-1623, Japan.
³ Department of Agriculture, School of Agriculture, Tokai University, Kumamoto 862-8652, Japan.
⁴ Faculty of Agriculture, Iwate University, 3-18-8 Ueda, Morioka, Iwate 020-8550, Japan.

PMID: 38318875
DOI: 10.1093/plphys/kiae059

Abstract

The inflorescence (spadix) of skunk cabbage (Symplocarpus renifolius) is strongly thermogenic and can regulate its temperature at around 23°C even when the ambient temperature drops below freezing. To elucidate the mechanisms underlying developmentally controlled thermogenesis and thermoregulation in skunk cabbage, we conducted a comprehensive transcriptome and metabolome analysis across three developmental stages of spadix development. Our RNA-seq analysis revealed distinct groups of expressed genes, with selenium-binding protein 1/methanethiol oxidase (SBP1/MTO) exhibiting the highest levels in thermogenic florets. Notably, the expression of alternative oxidase (AOX) was consistently high from the pre-thermogenic stage through the thermogenic stage in the florets. Metabolome analysis showed that alterations in nucleotide levels correspond with the developmentally controlled and tissue-specific thermogenesis of skunk cabbage, evident by a substantial increase in AMP levels in thermogenic florets. Our study also reveals that hydrogen sulfide, a product of SBP1/MTO, inhibits cytochrome c (COX)-mediated mitochondrial respiration while AOX-mediated respiration remains relatively unaffected. Specifically, at lower temperatures, the inhibitory effect of hydrogen sulfide on COX-mediated respiration increases, promoting a shift towards the dominance of AOX-mediated respiration. Finally, despite the differential regulation of genes and metabolites throughout spadix development, we observed a convergence of gene expression and metabolite accumulation patterns during thermogenesis. This synchrony may play a key role in developmentally regulated thermogenesis. Moreover, such convergence during the thermogenic stage in the spadix may provide a solid molecular basis for thermoregulation in skunk cabbage.

Keywords: AMP; RNA-seq; Thermogenic plants; alternative oxidase; metabolome; respiration; selenium-binding protein 1/methanethiol oxidase.