Exploring cotton SFR2's conundrum in response to cold stress.

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.

Oligogalactolipid production during cold challenge is conserved in early diverging lineages.

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.

An adaptive teosinte mexicana introgression modulates phosphatidylcholine levels and is associated with maize flowering time.

Native Americans domesticated maize (Zea mays ssp. mays) from lowland teosinte parviglumis (Zea mays ssp. parviglumis) in the warm Mexican southwest and brought it to the highlands of Mexico and South America where it was exposed to lower temperatures that imposed strong selection on flowering time. Phospholipids are important metabolites in plant responses to low-temperature and phosphorus availability and have been suggested to influence flowering time. Here, we combined linkage mapping with genome scans to identify High PhosphatidylCholine 1 (HPC1), a gene that encodes a phospholipase A1 enzyme, as a major driver of phospholipid variation in highland maize. Common garden experiments demonstrated strong genotype-by-environment interactions associated with variation at HPC1, with the highland HPC1 allele leading to higher fitness in highlands, possibly by hastening flowering. The highland maize HPC1 variant resulted in impaired function of the encoded protein due to a polymorphism in a highly conserved sequence. A meta-analysis across HPC1 orthologs indicated a strong association between the identity of the amino acid at this position and optimal growth in prokaryotes. Mutagenesis of HPC1 via genome editing validated its role in regulating phospholipid metabolism. Finally, we showed that the highland HPC1 allele entered cultivated maize by introgression from the wild highland teosinte Zea mays ssp. mexicana and has been maintained in maize breeding lines from the Northern United States, Canada, and Europe. Thus, HPC1 introgressed from teosinte mexicana underlies a large metabolic QTL that modulates phosphatidylcholine levels and has an adaptive effect at least in part via induction of early flowering time.

The arches and spandrels of maize domestication, adaptation, and improvement.

People living in the Balsas River basin in southwest México domesticated maize from the bushy grass teosinte. Nine thousand years later, in 2021, Ms. Deb Haaland - a member of the Pueblo of Laguna tribe of New Mexico - wore a dress adorned with a cornstalk when she was sworn in as the Secretary of Interior of the United States of America. This choice of garment highlights the importance of the coevolution of maize and the farmers who, through careful selection over thousands of years, domesticated maize and adapted the physiology and shoot architecture of maize to fit local environments and growth habits. Some traits such as tillering were directly selected on (arches), and others such as tassel size are the by-products (spandrels) of maize evolution. Here, we review current knowledge of the underlying cellular, developmental, physiological, and metabolic processes that were selected by farmers and breeders, which have positioned maize as a top global staple crop.

An Arabidopsis protoplast isolation method reduces cytosolic acidification and activation of the chloroplast stress sensor SENSITIVE TO FREEZING 2.

Chloroplasts adapt to freezing and other abiotic stresses in part by modifying their membranes. One key-remodeling enzyme is SENSITIVE TO FREEZING2 (SFR2). SFR2 is unusual because it does not respond to initial cold stress or cold acclimation, instead it responds during freezing conditions in Arabidopsis. This response has been shown to be sensitive to cytosolic acidification. The unique lipid products of SFR2 have also been detected in response to non-freezing stresses, but what causes SFR2 to respond in these stresses is unknown. Here, we investigate protoplast isolation as a representative of wounding stress. We show that SFR2 oligogalactolipid products accumulate during protoplast isolation. Notably, we show that protoplast cytosol is acidified during isolation. Modification of the buffers reduces oligogalactolipid accumulation, while prolonged incubation in the isolated state increases it. We conclude that SFR2 activation during protoplast isolation correlates with cytosolic acidification, implying that all SFR2 activation may be dependent on cytosolic acidification. We also conclude that protoplasts can be more gently isolated, reducing their stress.

Low-temperature tolerance in land plants: Are transcript and membrane responses conserved?

Plants' tolerance of low temperatures is an economically and ecologically important limitation on geographic distributions and growing seasons. Tolerance for low temperatures varies significantly across different plant species, and different mechanisms likely act in different species. In order to survive low-temperature stress, plant membranes must maintain their fluidity in increasingly cold and oxidative cellular environments. The responses of different species to low-temperature stress include changes to the types and desaturation levels of membrane lipids, though the precise lipids affected tend to vary by species. Regulation of membrane dynamics and other low-temperature tolerance factors are controlled by both transcriptional and post-transcriptional mechanisms. Here, we review low-temperature induced changes in both membrane lipid composition and gene transcription across multiple related plant species with differing degrees of low-temperature tolerance. We attempt to define a core set of changes for transcripts and lipids across species and treatment variations. Some responses appear to be consistent across all species for which data are available, while many others appear likely to be species or family-specific. Potential rationales are presented, including variance in testing, reporting and the importance of considering the level of stress perceived by the plant.

Lipid transport required to make lipids of photosynthetic membranes.

Photosynthetic membranes provide much of the usable energy for life on earth. To produce photosynthetic membrane lipids, multiple transport steps are required, including fatty acid export from the chloroplast stroma to the endoplasmic reticulum, and lipid transport from the endoplasmic reticulum to the chloroplast envelope membranes. Transport of hydrophobic molecules through aqueous space is energetically unfavorable and must be catalyzed by dedicated enzymes, frequently on specialized membrane structures. Here, we review photosynthetic membrane lipid transport to the chloroplast in the context of photosynthetic membrane lipid synthesis. We independently consider the identity of transported lipids, the proteinaceous transport components, and membrane structures which may allow efficient transport. Recent advances in lipid transport of chloroplasts, bacteria, and other systems strongly suggest that lipid transport is achieved by multiple mechanisms which include membrane contact sites with specialized protein machinery. This machinery is likely to include the TGD1, 2, 3 complex with the TGD5 and TGD4/LPTD1 systems, and may also include a number of proteins with domains similar to other membrane contact site lipid-binding proteins. Importantly, the likelihood of membrane contact sites does not preclude lipid transport by other mechanisms including vectorial acylation and vesicle transport. Substantial progress is needed to fully understand all photosynthetic membrane lipid transport processes and how they are integrated.

Chloroplast Membrane Remodeling during Freezing Stress Is Accompanied by Cytoplasmic Acidification Activating SENSITIVE TO FREEZING2.

Low temperature is a seasonal abiotic stress that restricts native plant ranges and crop distributions. Two types of low-temperature stress can be distinguished: chilling and freezing. Much work has been done on the mechanisms by which chilling is sensed, but relatively little is known about how plants sense freezing. Recently, Arabidopsis (Arabidopsis thaliana) SENSITIVE TO FREEZING2 (SFR2) was identified as a protein that responds in a nontranscriptional manner to freezing. Here, we investigate the cellular conditions that allow SFR2 activation. Using a combination of isolated organelle, whole-tissue, and whole-plant assays, we provide evidence that SFR2 is activated by changes in cytosolic pH and Mg(2+) Manipulation of pH and Mg(2+) in cold-acclimated plants is shown to cause changes similar to those of freezing. We conclude that pH and Mg(2+) are perceived as intracellular cues as part of the sensing mechanism for freezing conditions. This evidence provides a specific molecular mechanism to combat freezing.