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Influence of Extremely Low Temperatures of the Pole of Cold on the Lipid and Fatty-Acid Composition of Aerial Parts of the Horse

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Influence of Extremely Low Temperatures of the Pole of Cold on the Lipid and Fatty-Acid Composition of Aerial Parts of the Horse plants Article Influence of Extremely Low Temperatures of the Pole of Cold on the Lipid and Fatty-Acid Composition of Aerial Parts of the Horsetail Family (Equisetaceae) Vasiliy V. Nokhsorov 1,*, Lyubov V. Dudareva 2 , Svetlana V. Senik 3, Nadezhda K. Chirikova 1 and Klim A. Petrov 4 1 Institute of Natural Sciences, North-Eastern Federal University, 48 Kulakovskogo Str., 677000 Yakutsk, Russia; [email protected] 2 Laboratory of Physical and Chemical Research Methods, Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch of Russian Academy of Sciences, 132 Lermontova Str., 664033 Irkutsk, Russia; laser@sifibr.irk.ru 3 Laboratory of Fungal Biochemistry, Komarov Botanical Institute, Russian Academy of Sciences, 2 Professor Popov Str., 197376 St. Petersburg, Russia; [email protected] 4 Laboratory of Biogeochemical Cycles of Permafrost Ecosystems, Institute for Biological Problems of Cryolithozone of Siberian Branch of the Russian Academy of Sciences, 41 Lenina Av., 677000 Yakutsk, Russia; [email protected] * Correspondence: [email protected] Abstract: The lipid composition of two species of vascular plants, Equisetum variegatum Schleich. ex. Web. and E. scirpoides Michx., growing in the permafrost zone (Northeastern Yakutia, the Pole of Cold Citation: Nokhsorov, V.V.; Dudareva, of the Northern Hemisphere), with average daily air temperatures in summer of +17.8 ◦C, in autumn L.V.; Senik, S.V.; Chirikova, N.K.; of +0.6 ◦C, and in winter of −46.7 ◦C, was comparatively studied. The most significant seasonal Petrov, K.A. Influence of Extremely trend of lipid composition was an accumulation of PA in both horsetail species in the autumn– Low Temperatures of the Pole of Cold winter period. Cold acclimation in autumn was accompanied by a decrease in the proportion of on the Lipid and Fatty-Acid bilayer-forming lipids (phosphatidylcholine in the non-photosynthetic membranes and MGDG in Composition of Aerial Parts of the photosynthetic membranes), an increase in the desaturation degree due to the accumulation of Horsetail Family (Equisetaceae). E. scirpoides O N N N Plants 2021, 10, 996. https:// triene fatty acids ( ), and an accumulation of betaine lipids -(1,2-diacylglycero)- , , - doi.org/10.3390/plants10050996 trimethylhomoserine (DGTS). The inverse changes in some parameters were registered in the winter period, including an increase in the proportion of “bilayer” lipids and decrease in the unsaturation Academic Editors: Ryozo Imai and degree. According to the data obtained, it can be concluded that high levels of accumulation of Gabor Galiba membrane lipids and polyunsaturated FAs (PUFAs), as well as the presence of D5 FAs in lipids, are apparently features of cold hardening of perennial herbaceous plants in the cryolithozone. Received: 8 April 2021 Accepted: 13 May 2021 Keywords: Equisetum variegatum; Equisetum scirpoides; horsetails; low temperatures; hardening; Published: 17 May 2021 phospholipids; glycolipids; betaine lipids; DGTS; fatty acids; seasonal dynamics; the Pole of Cold Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- 1. Introduction iations. The study of organisms adapting to extreme environmental conditions is one of the important problems of modern biology. Northeastern Yakutia is a physico-geographical region with severe and very diverse living conditions. The Pole of Cold of the Northern Hemisphere is located here. The entire region lies in the permafrost zone, the thickness of Copyright: © 2021 by the authors. which exceeds 600 m in some places. Many plant species inhabiting Northeastern Yakutia Licensee MDPI, Basel, Switzerland. grow there at their distribution limit. This article is an open access article The specificity of the seasonal growth of the bulk of the herbaceous vegetation in distributed under the terms and Northeastern Yakutia is that it develops intensively in the first half of summer in order to conditions of the Creative Commons Attribution (CC BY) license (https:// have time to go through a complete vegetation cycle and give full-fledged seeds. How- creativecommons.org/licenses/by/ ever, horsetail meadows, especially those consisting of variegated horsetail (E. variegatum) 4.0/). Plants 2021, 10, 996. https://doi.org/10.3390/plants10050996 https://www.mdpi.com/journal/plants PlantsPlants 20212021,, 1010,, 996x FOR PEER REVIEW 22 of of 1415 (Figureconditions,1) , are they often do not subjected have time to long-term to go thro hardeningugh the complete by floodwaters. vegetation Under cycle. these When condi- the wintertions, they season do notbegins, have autumn-vegetating time to go through plan the completets get covered vegetation with snow cycle. with When their the wintershoots greenseason and begins, acquire autumn-vegetating the ability to accumulate plants get relatively covered more with storage snow with lipids their and shoots other greennutri- entsand acquire[1,2]. the ability to accumulate relatively more storage lipids and other nutrients [1,2]. (A) (B) Figure 1.1. Summer-growing shoots of Equisetum variegatum (A)) andand Equisetum scirpoides ((B) growinggrowing atat thethe PolePole ofof ColdCold ofof thethe NorthernNorthern Hemisphere.Hemisphere. At first first glance, it seems incredible that herbaceousherbaceous plants at the Pole of Cold manage to enrich enrich themselves themselves with with a alarge large number number of the of the most most energy- energy- and andmaterial-intensive material-intensive sub- stancessubstances during during the the growing growing season. season. Neverthele Nevertheless,ss, horsetails horsetails accumulate accumulate a a large large amount of proteins,proteins, carbohydrates,carbohydrates, and and lipids, lipids, and and they they become become an adaptivean adaptive fattening fattening food food for both for bothnon-hibernating non-hibernating and hibernating and hibernating herbivores herbiv in autumn,ores in autumn, winter, and winter, early and spring early [3,4 spring]. This [3,4].rapid This accumulation rapid accumulation of nutrients of isnutrients supported is supported by a complex by a ofcomplex evolutionary of evolutionary adaptations ad- aptationsto permafrost to permafrost conditions. conditions. For example, For weexample, previously we previously determined determined that E. variegatum that E. varie-(like E.gatum arvense (likeand E. arvenseE. scirpoides and E.) belongs scirpoides to) thebelongs group to of the 16:3 group plants of 16:3 in terms plants of in the terms content of the of contenttriene FAs. of triene Specifically, FAs. Specifically,D5 acids, including Δ5 acids, 5,11,14,17-eicosatetraenoic including 5,11,14,17-eicosatetraenoic acid (uniperonic), acid which(uniperonic), are characteristic which are ofcharacteristic evolutionarily of ancientevolutionarily taxa, were ancient identified taxa, inwere the identified FA composition in the FAof the composition aerial parts of of the horsetails. aerial parts Four of unsaturated horsetails. Four bonds unsaturated in this fatty bonds acid are in assumedthis fatty toacid be possiblyare assumed involved to be inpossibly the enhancement involved in of the plant enhancement tissue resistance of plant to low tissue temperatures. resistance to [5 low]. It wastemperatures. also found [5]. that, It inwas the also autumn, found when that, adapting in the autumn, to low ambient when adapting temperatures to low of ambient the Pole temperaturesof Cold in the of Northern the PoleHemisphere, of Cold in the horsetails Northern synthesize Hemisphere, a secondary horsetails keto synthesize carotenoid— a sec- ondaryrhodoxanthin. keto carotenoid—rhodoxa It was shown thatnthin. secondary It was shown carotenoids that se cancondary play acarotenoids special role can in play the aregulation special role of tolerancein the regulation to low temperatures of tolerance to in low some temperatures plant species in (for some instance, plant speciesEquisetum (for). Thus,instance, rhodoxanthin Equisetum). in Thus, some rhodoxanthin cases features in a some more importantcases features antioxidant a more important function than antiox- the xanthophyll cycle, which cannot operate at constantly low temperatures [6]. idant function than the xanthophyll cycle,◦ which cannot operate at constantly low tem- peraturesLow positive[6]. temperatures (0 + 10 C), named a cold spell, lead to acclimation (hard- ening).Low It positive is an adaptation temperatures response (0 + 10 during °C), named which a plants cold spell, trigger lead numerous to acclimation biochemical (hard- and physiological mechanisms necessary for acquiring frost resistance and survival in win- ening). It is an adaptation response during which plants trigger numerous biochemical ter [7,8]. Subzero temperatures (frosts) cause injuries in plant tissues due to the formation and physiological mechanisms necessary for acquiring frost resistance and survival in of ice crystals. The plasma membrane is considered to be the primary site of freezing injury winter [7,8]. Subzero temperatures (frosts) cause injuries in plant tissues due to the for- and, therefore, is subjected to restructuring during cold acclimation. According to modern mation of ice crystals. The plasma membrane is considered to be the primary site of freez- concepts, the relative abundance and saturation level of membrane lipids play an impor- ing injury and, therefore, is subjected to restructuring during cold acclimation. According tant role in the process of plant adaptation to temperature stress. Phosphatidylcholine
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