Minor loading vein acclimation for three Arabidopsis thaliana ecotypes in response to growth under different temperature and light regimes

Abstract

In light of the important role of foliar phloem as the nexus between energy acquisition through photosynthesis and distribution of the products of photosynthesis to the rest of the plant, as well as communication between the whole plant and its leaves, we examined whether foliar minor loading veins in three Arabidopsis thaliana ecotypes undergo acclimation to the growth environment. As a winter annual exhibiting higher rates of photosynthesis in response to cooler vs. warmer temperatures, this species might be expected to adjust the structure of its phloem to accommodate greater fluxes of sugars in response to growth at low temperature. Minor (fourth- and third-order) veins had 14 or fewer sieve elements and phloem tissue comprised 50% or more of the cross-sectional area. The number of phloem cells per minor loading vein was greater in leaves grown under cool temperature and high light vs. warm temperature and moderate light. This effect was greatest in an ecotype from Sweden, in which growth under cool temperature and high light resulted in minor veins with an even greater emphasis on phloem (50% more phloem cells with more than 100% greater cross-sectional area of phloem) compared to growth under warm temperature and moderate light. Likewise, the number of sieve elements per minor vein increased linearly with growth temperature under moderate light, almost doubling over a 27°C temperature range (21°C leaf temperature range) in the Swedish ecotype. Increased emphasis on cells involved in sugar loading and transport may be critical for maintaining sugar export from leaves of an overwintering annual such as A. thaliana, and particularly for the ecotype from the northern-most population experiencing the lowest temperatures.

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

“…Decreased tocopherol levels at the end of the photoperiod and a lesser maximal NPQ capacity under experimental high-light exposure in the Italian ecotype suggest the possibility that this ecotype may be genetically programmed to allow a greater generation of redox-dependent signals, resulting from both less detoxification of ROS (via tocopherol) and less preemptive counteraction of ROS formation (via thermal dissipation). Future studies should explore the possibility that redoxdependent signaling networks provide input for genetic differences in leaf development in the Swedish versus the Italian ecotypes (Cohu et al 2013a, b;Adams et al 2014) and that a possible difference in the set-point of ROS formation (perhaps via differential expression of the NPQcontrolling PsbS protein, the protein S of photosystem II, required for rapidly reversible dissipation of excess absorbed light [Li et al 2009] and/or genes in tocopherol biosynthesis) between these two ecotypes may be one of the mechanisms of ecotypic adaptation to the environment.…”

“…While leaves of both ecotypes exhibited a strong response to growth at low temperature under high light, consisting of a greater number of phloem cells per minor vein and record high rates of photosynthetic oxygen evolution (Cohu et al 2013a, b), the Swedish ecotype had even more numerous minor vein phloem cells (Cohu et al 2013a), more pronounced phloem parenchyma cell wall ingrowths (presumably providing for a greater number of phloem parenchyma cell membrane localized ATPases and sucrose-efflux transporters important for the active loading of sucrose into the sieve elements; Adams et al 2014), and higher photosynthetic capacities (Cohu et al 2013b;Adams et al 2014) compared to the Italian ecotype when both were grown under moderate light at low temperature. Moreover, these two ecotypes, and hundreds of inbred lines derived from these two parents, have been used to dissect genes underlying the control of flowering and others involved in fitness and potential trade-offs in fitness (Å gren et al 2013;Grillo et al 2013;Dittmar et al 2014;Oakley et al 2014).…”

Multiple feedbacks between chloroplast and whole plant in the context of plant adaptation and acclimation to the environment

“…Only the Swedish ecotype responded to a decrease in growth temperature (without an increase in growth light intensity) with an increase in the size of the sieve tubes of the leaves' minor veins (figure 3; see also [80,81]). A combination of both low temperature and high light during plant growth was required to elicit a similar response in the Italian ecotype (figure 3; see also [80,81]). These findings suggest that the two ecotypes of this winter annual species do not differ in the principal ability to adjust leaf anatomy to cool growth temperature, but do differ in the intensity of cues required to elicit such a response.…”

“…These responses are featured in figures 1 and 2 as (increased, decreased or genetically limited) carbon export capacity (phloem loading/ sugar transport) and photosynthetic capacity. Firstly, it was shown that number and size of the cells loading sugars into the phloem's sugar-transporting sieve tubes as well as number and size of the sieve tubes are adjusted to growth temperature in the winter annual species Arabidopsis and spinach [79][80][81]. The characterized winter annuals typically germinate in the autumn, overwinter as rosettes, and complete their life cycle in the following spring.…”

“…In addition to being the site of the above-described occlusion (table 1 and figure 1) in the possible service of defence against pathogens that spread through the phloem, phloem-loading complexes were recently proposed to be the target point for overall adjustment of foliar carbon export capacity in response to environmental change [79,80]. Differences in the adjustability of phloem loading and carbon export were, furthermore, shown to be excellent predictors for differences in photosynthetic acclimation to the environment between plant varieties (ecotypes) and species from different geographical regions [81].…”