Leaf architectural, vascular and photosynthetic acclimation to temperature in two biennials

Abstract

Acclimation of leaf features to growth temperature was investigated in two biennials (whose life cycle spans summer and winter seasons) using different mechanisms of sugar loading into exporting conduits, Verbascum phoeniceum (employs sugar-synthesizing enzymes driving symplastic loading through plasmodesmatal wall pores of phloem cells) and Malva neglecta (likely apoplastic loader transporting sugar via membrane transport proteins of phloem cells). In both species, acclimation to lower temperature involved greater maximal photosynthesis rates and vein density per leaf area in close correlation with modification of minor vein cellular features. While the symplastically loading biennial exhibited adjustments in the size of minor leaf vein cells (consistent with adjustment of the level of sugar-synthesizing enzymes), the putative apoplastic biennial exhibited adjustments in the number of cells (consistent with adjustment of cell membrane area for transporter placement). This upregulation of morphological and anatomical features at lower growth temperature likely contributes to the success of both the species during the winter. Furthermore, while acclimation to low temperature involved greater leaf mass per area in both species, this resulted from greater leaf thickness in V. phoeniceum vs a greater number of mesophyll cells per leaf area in M. neglecta. Both types of adjustments presumably accommodate more chloroplasts per leaf area contributing to photosynthesis. Both biennials exhibited high foliar vein densities (particularly the solar-tracking M. neglecta), which should aid both sugar export from and delivery of water to the leaves.

Growth temperature impact on leaf form and function in Arabidopsis thaliana ecotypes from northern and southern Europe

“…; Muller et al . ). Extraction of chlorophylls and tocopherols (from three to five leaf discs from three to five plants) followed by quantification using high‐performance liquid chromatography was as described in Stewart et al .…”

“…,, ; Muller et al . ). A greater number of sieve elements provide a greater cross‐sectional area through which sugars can flux out of the leaf, and the greater number of all phloem cells provides for a greater membrane area for sucrose flux channels (phloem parenchyma cells [PC]), ATPases (PC and companion cells [CC]), and proton‐sucrose symporters (CC and sieve elements) that facilitate active loading of sucrose into the sieve elements in apoplastic loaders like A. thaliana (Duan et al .…”

“…; Muller et al . ), as well as an apparent increased capacity for foliar sugar export facilitated by greater numbers of minor vein phloem cells (Adams et al . ; Cohu et al .…”

Differences in light-harvesting, acclimation to growth-light environment, and leaf structural development between Swedish and Italian ecotypes of Arabidopsis thaliana

“…Anderson et al (1995) noted that, ''growth at low temperature mimics high light acclimation'' and suggested that similar triggers (associated with cellular redox-signaling networks; see below) are involved (for a recent review, see Hüner et al 2012). Increases in leaf thickness in response to cold growth temperature have been reported for several biennial and winter annual species (Boese and Huner 1990;Gorsuch et al 2010;Dumlao et al 2012;Cohu et al 2014a;Muller et al 2014). Various changes in foliar structure and function in response to cold temperature are coordinated by the transcription factor family CBF (for C-repeat-binding factor) in Arabidopsis and other species (Thomashow 1999(Thomashow , 2001(Thomashow , 2010Carvallo et al 2011;Dong et al 2011;Dahal et al 2012;Lee and Thomashow 2012; see also Agarwal et al 2006;Medina et al 2011).…”

“…Light-and CO 2 -saturated photosynthesis and leaf thickness measurements Measurements of P max (photosynthetic capacity, as the light-and CO 2 -saturated rate of oxygen evolution at 25°C), leaf dry mass per unit leaf area (LMA), leaf and palisade mesophyll thickness, number of palisade mesophyll cell layers, and sample preparation for microscopy were conducted as previously described (Amiard et al 2005;Dumlao et al 2012;Muller et al 2014). Photosynthetic oxygen evolution from excised leaf tissue was measured in a temperature-controlled leaf-disk oxygen electrode chamber in water-saturated air and 5 % CO 2 , which eliminates cuticular, stomatal, and mesophyll resistance to CO 2 diffusion (Delieu and Walker 1981).…”