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Abstract Sulfate-proton co-transporters (SULTRs) mediate sulfate uptake, transport, storage, and assimilation in plants. The SULTR family has historically been classified into four groups (SULTR1-SULTR4), with well-characterized roles for SULTR groups 1, 2, and 4. However, the functions of the large and diverse SULTR3 group remain poorly understood. Here, we present an updated phylogenetic analysis of SULTRs across angiosperms, including multiple early-divergent lineages. Our results suggest that the enigmatic SULTR3 group comprises four distinct subfamilies that predate the emergence of angiosperms, providing a basis for reclassifying the SULTR family into seven subfamilies. This expanded classification is supported by subfamily-specific gene structures and amino acid substitutions in the substrate-binding pocket. Structural modeling identified three serine residues uniquely lining the substrate-binding pocket of SULTR3.4, enabling three hydrogen bonds with the phosphate ion. The data support the proposed neofunctionalization of this subfamily for phosphate allocation within vascular tissues. Transcriptome analysis of Populus tremula × alba revealed divergent tissue expression preferences among SULTR subfamilies and between genome duplicates. We observed partitioned expression in vascular tissues among the four SULTR3 subfamilies, with PtaSULTR3.4a and PtaSULTR3.2a preferentially expressed in primary and secondary xylem, respectively. Gene coexpression analysis revealed coordinated expression of PtaSULTR3.4a with genes involved in phosphate starvation responses and nutrient transport, consistent with a potential role in phosphate homeostasis. In contrast, PtaSULTR3.2a was strongly coexpressed with lignification and one-carbon metabolism genes and their upstream transcription regulators. PtaSULTR3.2a belongs to a eudicot-specific branch of the SULTR3.1 subfamily found only in perennial species, suggesting a specialized role in lignifying tissues. Together, our findings provide a refined phylogenetic framework for the SULTR family and suggest that the expanded SULTR3 subfamilies have undergone neofunctionalization during the evolution of vascular and perennial plants. 

Cotton is an important agricultural crop to many regions across the globe but is sensitive to low-temperature exposure. The activity of the enzyme SENSITIVE TO FREEZING 2 (SFR2) improves cold tolerance of plants and produces trigalactosylsyldiacylglycerol (TGDG), but its role in cold sensitive plants, such as cotton remains unknown. Recently, it was reported that cotton SFR2 produced very little TGDG under normal and cold conditions. Here, we investigate cotton SFR2 activation and TGDG production. Using multiple approaches in the native system and transformation into Arabidopsis thaliana, as well as heterologous yeast expression, we provide evidence that cotton SFR2 activates differently than previously found among other plant species. We conclude with the hypothesis that SFR2 in cotton is not activated in a similar manner regarding acidification or freezing like Arabidopsis and that other regions of SFR2 protein are critical for activation of the enzyme than previously reported. 

Abstract Severe cold, defined as a damaging cold beyond acclimation temperatures, has unique responses, but the signaling and evolution of these responses are not well understood. Production of oligogalactolipids, which is triggered by cytosolic acidification in Arabidopsis (Arabidopsis thaliana), contributes to survival in severe cold. Here, we investigated oligogalactolipid production in species from bryophytes to angiosperms. Production of oligogalactolipids differed within each clade, suggesting multiple evolutionary origins of severe cold tolerance. We also observed greater oligogalactolipid production in control samples than in temperature-challenged samples of some species. Further examination of representative species revealed a tight association between temperature, damage, and oligogalactolipid production that scaled with the cold tolerance of each species. Based on oligogalactolipid production and transcript changes, multiple angiosperm species share a signal of oligogalactolipid production initially described in Arabidopsis, namely cytosolic acidification. Together, these data suggest that oligogalactolipid production is a severe cold response that originated from an ancestral damage response that remains in many land plant lineages and that cytosolic acidification may be a common signaling mechanism for its activation.