Distinct Cold Acclimation of Productivity Traits in Arabidopsis thaliana Ecotypes

Abstract

Improvement of crop climate resilience will require an understanding of whole-plant adaptation to specific local environments. This review places features of plant form and function related to photosynthetic productivity, as well as associated gene-expression patterns, into the context of the adaptation of Arabidopsis thaliana ecotypes to local environments with different climates in Sweden and Italy. The growth of plants under common cool conditions resulted in a proportionally greater emphasis on the maintenance of photosynthetic activity in the Swedish ecotype. This is compared to a greater emphasis on downregulation of light-harvesting antenna size and upregulation of a host of antioxidant enzymes in the Italian ecotype under these conditions. This differential response is discussed in the context of the climatic patterns of the ecotypes' native habitats with substantial opportunity for photosynthetic productivity under mild temperatures in Italy but not in Sweden. The Swedish ecotype's response is likened to pushing forward at full speed with productivity under low temperature versus the Italian ecotype's response of staying safe from harm (maintaining redox homeostasis) while letting productivity decline when temperatures are transiently cold. It is concluded that either strategy can offer directions for the development of climate-resilient crops for specific locations of cultivation.

Keywords: Lhcb; daylength; excitation pressure; freezing; growth; high light; nonphotochemical quenching; phloem; photosynthetic capacity; xylem.

Figure 1

(A) Map showing the geographic origins of the SW (blue square; 62°48′ N, 18°12′ E) and IT (red circle; 42°07′ N, 12°29′ E) A. thaliana ecotypes (after [37]) as well as (B,C) the change in day length and (D,E) monthly minimal (closed symbols) and maximal (open symbols) temperatures across the growing season (light blue or red shading) for (B,D) SW and (C,E) IT at their respective sites of origin. Data on growing seasons for the two ecotypes from [41,46].

Figure 2

Schematic depiction of relative differences in capacities for light-harvesting (antenna), photoprotective dissipation of excess excitation energy as heat, electron transport, carbon dioxide fixation, sugar export (sucrose symbol), and ROS production and detoxification in leaves of the (A) SW and (B) IT ecotypes of A. thaliana.

Figure 3

(A) Light- and CO₂-saturated capacity of photosynthesis measured at 25 °C and (B) chlorophyll a/b ratio in IT (red columns) and SW (blue columns) plants grown under a cool temperature and high light (data from [52]), moderate temperature and high light (data from [59]), and cool temperature and moderate light (data from [24,57]). Mean values ± standard deviations (n = 3 or 4); statistically significant differences between ecotypes based on Student’s t-tests are indicated with asterisks (* = p < 0.05; ** = p < 0.01; *** = p < 0.001); n.s. = not significantly different.

Figure 4

Minor-vein (A) phloem and (B) xylem volumes on a leaf area basis for IT (red columns) and SW (blue columns) grown under a cool temperature and high light (data from [24]), moderate temperature and high light (data from [59]), and cool temperature and moderate light (recalculated data from [24]). Mean values ± standard deviations (n = 3 or 4); statistically significant differences between ecotypes based on Student’s t-tests are indicated with asterisks (* = p < 0.05; ** = p < 0.01); n.s. = not significantly different.

Figure 5

Thermal energy dissipation quantified from non-photochemical quenching (NPQ) of chlorophyll fluorescence in IT (red circles and columns) and SW (blue squares and columns) ecotypes (A) upon transfer to cold temperature (4 °C) and high light (800 µmol photons m⁻² s⁻¹) following growth at warm temperatures and low light (re-graphed from [50]), and (B) at the end of a 5 min exposure to high light (800 µmol photons m⁻² s⁻¹) as well as (C) under measuring conditions of saturating light (over 2000 µmol photons m⁻² s⁻¹) following growth at warm temperature (25 °C) and low light (200 µmol photons m⁻² s⁻¹) with and without 5 min daily high light periods (pulses) (data from [56]). Mean values ± standard deviations (n = 4); statistically significant differences between ecotypes based on Student’s t-tests are indicated with asterisks (* = p < 0.05; *** = p < 0.001); n.s. = not significantly different.

Figure 6

Excitation pressure as assessed from the reduction state of the primary electron acceptor Q_A of photosystem II (via chlorophyll fluorescence [77]) measured under either low light (50 µmol photons m⁻² s⁻¹) or saturating light (2000 µmol photons m⁻² s⁻¹) in IT (red columns) and SW (blue columns) grown under cool temperature and high light. Mean values ± standard deviations (n = 3); statistically significant differences between ecotypes based on Student’s t-tests are indicated with asterisks (*** = p < 0.001). Data from [52].

Figure 7

Gene expression patterns of either up- or downregulation in plants of IT and SW grown under high light and cold temperature (HLC) versus low light and warm temperature (LLW) for (A) several proteins of the light-harvesting chlorophyll (a + b)-binding (LHCB) family, including LHCB1.1 (AT1G29920); LHCB1.2 (AT1G29910); LHCB1.3 (AT1G29930); LHCB1.4 (AT2G34430), and LHCB1.5 (AT2G34420) as well as (B,C), selected antioxidant enzymes, including class III peroxidases PRX33 (AT3G49110) and PRX34 (AT3G49120), glutathione S-transferases GST1 (AT1G02930) and GST11 (AT1G02920), glutathione peroxidase GPX6 (AT4G11600), cytosolic thioredoxin TRX5 (AT1G45145), stromal ascorbate peroxidase SAPX (AT4G08390) and ascorbate peroxidase APX1 (ATG07890), and iron superoxide dismutase SOD3 (AT5G23310). Significant up- or down-regulation between growth conditions are indicated with asterisks (* = p < 0.05; ** = p < 0.01; *** = p < 0.001); n.s. = not significantly different. Data from [52].