A discordance of seasonally covarying cues uncovers misregulated phenotypes in the heterophyllous pitcher plantCephalotus follicularis

Abstract

Organisms withstand normal ranges of environmental fluctuations by producing a set of phenotypes genetically programmed as a reaction norm; however, extreme conditions can expose a misregulation of phenotypes called a hidden reaction norm. Although an environment consists of multiple factors, how combinations of these factors influence a reaction norm is not well understood. To elucidate the combinatorial effects of environmental factors, we studied the leaf shape plasticity of the carnivorous pitcher plant Cephalotus follicularis . Clonally propagated plants were subjected to 12-week-long growth experiments in different conditions controlled by growth chambers. Here, we show that the dimorphic response of forming a photosynthetic flat leaf or an insect-trapping pitcher leaf is regulated by two covarying environmental cues: temperature and photoperiod. Even within the normal ranges of temperature and photoperiod, unusual combinations of the two induced the production of malformed leaves that were rarely observed under the environmentally typical combinations. We identified such cases in combinations of a summer temperature with a short-to-neutral day length, whose average frequency in the natural Cephalotus habitats corresponded to a once-in-a-lifetime event for this perennial species. Our results suggest that even if individual cues are within the range of natural fluctuations, a hidden reaction norm can be exposed under their discordant combinations. We anticipate that climate change may challenge organismal responses through not only extreme cues but also through uncommon combinations of benign cues.

Replicated radiations in the South American Marsh Pitcher genus Heliamphora (Sarraceniaceae) lead to convergent carnivorous trap morphologies

“…Pitchers growing in heavy shade typically lose carnivorous activity and function primarily as photosynthetic structures, as indicated by the elongated pitcher bodies, and the absence of pitcher coloration, nectar spoon structure, or attractants . Similar plastic responses are found in Darlingtonia, Sarracenia and all other pitcher plants, suggesting pitcher plasticity commonly associated with trade-offs between carnivory and photosynthesis (Givnish et al 1984;Ellison and Gotelli 2002;Ellison and Farnsworth 2005;Pavlovič and Saganová 2015;Givnish et al 2018;Fukushima et al 2021).…”

“…Like all leaves, the pitcher development is plastic and can be affected by many environmental factors (Brewer 1999;Ellison and Gotelli 2002;Fukushima et al 2021). This is the first study to examine plasticity in Heliamphora pitcher rosette development, and we focused on a condition that is common in nature -crowding due to the presence of neighboring plants.…”

The digestive systems of carnivorous plants

“…Not much is known about the tissue-specific secretion and localization of digestive enzymes, except for the phosphatases and the aspartic protease Nepenthesin I expressed in the parenchyma around the glands of Nepenthes ( Athauda et al, 2004 ). In Cephalotus , which conditionally produces distinct trapping leaves (Fukushima et al, 2017 , 2021 ), approximately half of the genes encoding digestive fluid proteins are specifically expressed in pitcher leaves, but the other half are also expressed in the photosynthetic, nontrapping leaves ( Fukushima et al, 2017 ). Trap-preferential gene expression has been reported in other species as well, with a few exceptions (Rottloff et al, 2011 , 2013 ; Nishimura et al, 2013 ; Arai et al, 2021 ).…”

Replicated radiations in the South American marsh pitcher plants (Heliamphora) lead to convergent carnivorous trap morphologies

“…Like all leaves, the pitcher development is plastic and can be affected by various environmental factors (Brewer, 1999; Ellison and Gotelli, 2002; Fukushima et al, 2021). This is the first study to examine plasticity in Heliamphora pitcher rosette development, specifically focusing on a common natural condition—crowding due to the presence of neighboring plants.…”