Adaptation in Unstable Environments and Global Gene Losses: Small but Stable Gene Networks by the May-Wigner Theory.

Although gene loss is common in evolution, it remains unclear whether it is an adaptive process. In a survey of seven major mangrove clades that are woody plants in the intertidal zones of daily environmental perturbations, we noticed that they generally evolved reduced gene numbers. We then focused on the largest clade of Rhizophoreae and observed the continual gene set reduction in each of the eight species. A great majority of gene losses are concentrated on environmental interaction processes, presumably to cope with the constant fluctuations in the tidal environments. Genes of the general processes for woody plants are largely retained. In particular, fewer gene losses are found in physiological traits such as viviparous seeds, high salinity, and high tannin content. Given the broad and continual genome reductions, we propose the May-Wigner theory (MWT) of system stability as a possible mechanism. In MWT, the most effective solution for buffering continual perturbations is to reduce the size of the system (or to weaken the total genic interactions). Mangroves are unique as immovable inhabitants of the compound environments in the land-sea interface, where environmental gradients (such as salinity) fluctuate constantly, often drastically. Extending MWT to gene regulatory network (GRN), computer simulations and transcriptome analyses support the stabilizing effects of smaller gene sets in mangroves vis-à-vis inland plants. In summary, we show the adaptive significance of gene losses in mangrove plants, including the specific role of promoting phenotype innovation and a general role in stabilizing GRN in unstable environments as predicted by MWT.

A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes.

Lectins interact with carbohydrates. They can function as pattern recognition receptors and play an important role in the innate immune system of animals. Previously, we have isolated two calcium-dependent (C-type) lectins, named immulectin-1 and -2, from the tobacco hornworm Manduca sexta. Both immulectin-1 and -2 stimulate prophenoloxidase activation in plasma. Here, we describe isolation and cDNA cloning of a novel member of immulectins, immulectin-3 (IML-3). IML-3, like immulectin-1 and -2, contains tandem carbohydrate-recognition domains (CRDs). The cDNA clone encoding IML-3 is 3802 bp long, with an open reading frame of 930 bp. This cDNA clone has an extremely long noncoding region at the 3' end that contains eight polyadenylation signal sequences. Northern analysis showed that a 5.0 kb IML-3 transcript was present in the fat body of control larvae (injected with saline) but not in the fat body of larvae injected with bacteria. However, a much more abundant 3.1 kb transcript was induced in the fat body of bacteria-injected larvae. IML-3 mRNA was not detected in hemocytes of control or bacteria-injected larvae. Recombinant IML-3 was expressed in bacteria and purified. It specifically bound to immobilized lipopolysaccharide (LPS) and lipoteichoic acid from bacteria, and to laminarin, a beta-1, 3-glucan. Binding of IML-3 to immobilized LPS was competed by excess free LPS. More importantly, IML-3 contains an anti-death-like motif in the carboxyl-terminal CRD. Endogenous IML-3 was detected in the cytoplasm of hemocytes, and FITC-labeled recombinant IML-3 was translocated from hemolymph into hemocytes. Coating of IML-3 onto agarose beads enhanced encapsulation of the beads.