Anisotropic contraction in forisomes: Simple models won't fit

Abstract

Forisomes are ATP-independent, Ca(2+)-driven contractile protein bodies acting as reversible valves in the phloem of plants of the legume family. Forisome contraction is anisotropic, as shrinkage in length is associated with radial expansion and vice versa. To test the hypothesis that changes in length and width are causally related, we monitored Ca(2+)- and pH-dependent deformations in the exceptionally large forisomes of Canavalia gladiata by high-speed photography, and computed time-courses of derived geometric parameters (including volume and surface area). Soybean forisomes, which in the resting state resemble those of Canavalia geometrically but have less than 2% of the volume, were also studied to identify size effects. Calcium induced sixfold volume increases in forisomes of both species; in soybean, responses were completed in 0.15 s, compared to about 0.5 s required for a rapid response in Canavalia followed by slow swelling for several minutes. This size-dependent behavior supports the idea that forisome contractility might rest on similar mechanisms as those of polyelectrolyte gels, a class of artificial "smart" materials. In both species, time-courses of forisome length and diameter were variable and lacked correlation, arguing against a simple causal relationship between changes in length and width. Moreover, changes in the geometry of soybean forisomes differed qualitatively between Ca(2+)- and pH-responses, suggesting that divalent cations and protons target different sites on the forisome proteins.

How phloem-feeding insects face the challenge of phloem-located defenses

“…They were suspected to undergo structural transformations, from a crystalloid state with co-aligned fibrils to a “slime-body” with dispersed fibrils (Palevitz and Newcomb, 1971). The transition is a rapid and reversible conformational change in which forisomes shorten longitudinally while expanding radially with a several-fold volume increase (Knoblauch et al, 2001; Peters et al, 2007, 2008). Forisomes disperse upon wounding and occlude sieve tubes (Knoblauch and van Bel, 1998), leading to a stop of mass flow observed in artificial sieve tubes (Knoblauch et al, 2012).…”

Sieve Tube Geometry in Relation to Phloem Flow

“…Phaseolus sieve elements contain forisomes, which rapidly occlude sieve plates in response to injury (Knoblauch et al, 2001;Peters et al, 2008). Cucurbita sieve tubes also contain P proteins, including the bestcharacterized P proteins, PP1 and PP2 (Bostwick et al, 1992;Golecki et al, 1999).…”

Münch, morphology, microfluidics - our structural problem with the phloem

“…More recently, it was demonstrated that this transition is in fact a reversible, rapid and anisotropic contractile reaction in which the protein body switches between a longitudinally expanded but radially contracted low-volume state, and a longitudinally contracted but radially expanded highvolume state (Fig. 4; compare Knoblauch et al 2001Knoblauch et al , 2003Peters, van Bel & Knoblauch 2006;Peters et al 2008). In the high-volume state, the protein bodies occlude the sieve tube at least partially .…”

“…The geometric anisotropy of forisome contractility in which expansion and contraction occur almost simultaneously along perpendicular geometric axes (Peters et al . 2008), together with the older terminology that referred to the apparent developmental stages as ‘condensed’ and ‘dispersed’, has led to a degree of linguistic confusion that occasionally renders descriptions of forisome behaviour almost incomprehensible (see, e.g.…”