Developmental changes and organelle biogenesis in the reproductive organs of thermogenic skunk cabbage (Symplocarpus renifolius)

Abstract

Sex-dependent thermogenesis during reproductive organ development in the inflorescence is a characteristic feature of some of the protogynous arum species. One such plant, skunk cabbage (Symplocarpus renifolius), can produce massive heat during the female stage but not during the subsequent male stage in which the stamen completes development, the anthers dehisce, and pollen is released. Unlike other thermogenic species, skunk cabbage belongs to the bisexual flower group. Although recent studies have identified the spadix as the thermogenic organ, it remains unclear how individual tissues or intracellular structures are involved in thermogenesis. In this study, reproductive organ development and organelle biogenesis were examined during the transition from the female to the male stage. During the female stage, the stamens exhibit extensive structural changes including changes in organelle structure and density. They accumulate high levels of mitochondrial proteins, including possible thermogenic factors, alternative oxidase, and uncoupling protein. By contrast, the petals and pistils do not undergo extensive changes during the female stage. However, they contain a larger number of mitochondria than during the male stage in which they develop large cytoplasmic vacuoles. Comparison between female and male spadices suggests that mitochondrial number rather than their level of activity correlates with thermogenesis. Their spadices, even in the male, contain a larger amount of mitochondria that had greater oxygen consumption, compared with non-thermogenic plants. Taken together, our data suggest that the extensive maturation process in stamens produces massive heat through increased metabolic activities. The possible mechanisms by which petal and pistil metabolism may affect thermogenesis are also discussed.

What is critical for plant thermogenesis? Differences in mitochondrial activity and protein expression between thermogenic and non-thermogenic skunk cabbages

“…Under both conditions, cyanide-resistant oxygen uptake was almost completely inhibited by the AOX inhibitor n-propyl gallate. When compared with the previously determined values for S. renifolius (Ito-Inaba et al 2009), all respiratory activities of state 2, 3, and alternative respiration from L. camtschatcensis were less than half those of S. renifolius. Taken together, these results suggest that lower mitochondrial density and respiratory activity may be correlated with the lack of thermogenesis in L. camtschatcensis.…”

“…In a previously published study (Ito-Inaba et al 2009), we found that mitochondrial density and respiratory activity in spadices of S. renifolius were much higher than in nonthermogenic plants, such as potato (Solanum tuberosoum L. cv. Danshaku) and cauliflower (Brassica oleracea L. botrytis).…”

“…It is therefore of great interest to determine whether these characteristic features of Symplocarpus are also found in the non-thermogenic Lysichiton. We purified mitochondria from the spadix of L. camtschatcensis and compared the mitochondrial density (Table 1) with the previously determined mitochondrial density value in S. renifolius (Ito-Inaba et al 2009). The mitochondrial density in L. camtschatcensis (0.011 ± 0.002 mg g -1 ) was much lower than that in S. renifolius (0.42 ± 0.14 mg g -1 ).…”

“…Although two UCP cDNAs encoding SrUCPA and SrUCPB were isolated from the spadix of S. renifolius, SrUCPA was identified as the major UCP by genomic, mRNA, and mass spectrometric analyses (Ito-Inaba et al 2008b). Using spadix mitochondria, the uncoupling activity of SrUCPA was analyzed using a membrane potential assay (Ito-Inaba et al 2008a), and the alternative respiration of SrAOX was measured using an oxygen consumption assay (Ito-Inaba et al 2009;Onda et al 2007). Two Cys residues, termed Cys I and Cys II , which are involved in modulating AOX activity through interactions with a-keto acids such as pyruvate, are conserved in SrAOX (Onda et al 2007).…”

“…It was also revealed that the mitochondrial density and respiratory activity in spadices of S. renifolius is much higher than in potato (Solanum tuberosum L. cv. Danshaku) roots and cauliflower (Brassica oleracea L. botrytis) infloresences which are both non-thermogenic plants (Ito-Inaba et al 2009). It is therefore of great interest to determine whether these characteristic features of Symplocarpus are also found in the non-thermogenic Lysichiton.…”