ISSN 00954527, Cytology and Genetics, 2015, Vol. 49, No. 2, pp. 139–145. © Allerton Press, Inc., 2015. Original Ukrainian Text © I.P. Ozheredova, I.Yu. Parnikoza, O.O. Poronnik, I.A. Kozeretska, S.V. Demidov, V.A. Kunakh, 2015, published in Tsitologiya i Genetika, 2015, Vol. 49, No. 2, pp. 72–79.

Mechanisms of Vascular Adaptation to Abiotic Environmental Factors I. P. Ozheredovaa, I. Yu. Parnikozab, O. O. Poronnikb, I. A. Kozeretskaa, S. V. Demidova, and V. A. Kunakhb aTaras Shevchenko National University, ul. Volodymyrska 64, Kyiv, 01033 Ukraine email: [email protected] bInstitute of Molecular Biology and Genetics, National Academy of Sciences of Ukraine, ul. Akademika Zabolotnoho 150, Kyiv, 03680 Ukraine Received November 21, 2013

Abstract—Native species of the Antarctic and quitensis exist at the limits of survival of vascular . Fundamental adaptations to abiotic environmental factors that qualitatively dis tinguish them from the other vascular plants of extreme regions, namely temperature, ultraviolet radiation hardiness, and their genetic plasticity in the changeable environment are discussed.

Keywords: , , Antarctic, mechanisms of adaptation, stress pro tein, genome plasticity DOI: 10.3103/S0095452715020085

INTRODUCTION surface that is connected with its level of adaptation to Plant adaptation concerns hereditarily fixed con conditions of certain habitat. Pearlworts is rather rare, stitutive properties typical for plants, regardless of the and the reasons for its limited spread are not explained fact whether they are in stressful conditions not. These enough [4, 9–13]. properties become apparent on the structural and bio Populations of these vascular plants grow on poor chemical level as well. In general, the problem of plant or, quite the contrary, overrich with semidecomposed adaptation to abiotic factors is of great ecological organics soils. They experience effects of severe envi importance, since plant ability to adapt to particular ronmental conditions—low temperature, ultraviolet conditions is one of factors determining the natural rays, and moisture deficit. During the direct analysis, habitat of wild plants and possibility of their introduc we studied some biological peculiarities of Antarctic tion [1]. The Antarctic is a unique place to study nat hair grass [4]. In our work, we pay attention to the con ural adaptation mechanisms. It is entirely isolated by temporary data concerning the reaction of native the South Ocean waters and the Polar Front system, plants to the main Antarctic abiotic factor because the and vascular plants live here in extreme conditions problems of specific adaptation mechanisms of Ant strained to the limits of their possibilities as 99.5% of arctic native plants are not clear. surface is covered with continent ice and 0.3% of its area is favorable for land ecosystems [2–6]. Such sec Growing on organic soils. Initial productivity (for tions include oases of continental or the Eastern Ant mation of plant biomass) depends on peculiarities of arctic and also the narrow western coast strip of the root nutrition of plants in land ecosystems of high lat Antarctic Peninsula and islands named the maritime itudes. In guanorich areas, the growth of plants differs Antarctic. If lichen, , and algae dominate in much in amount of nitrogen, which slowly releases severe surroundings, formations of Antarctic grass while decomposing because of low temperature. In the are spread in more favorable oases of the mari maritime Antarctic, D. antarctica and C. quitensis usu time Antarctic. The formations include two species of ally grow in guanorich territories rich particularly in native vascular plants—Antarctic hair grass (Des places of penguin rookery accumulations. This is champsia antarctica Desv., Poaceea) and Antarctic caused by a high level of nitratereductase activity of pearlworts (Colobanthus quitensis Kunth Bartl. Cary both species [14]. Thus, the ability to obtain nitrogen pophyllaceae) [4, 6–8]. These vascular plants are not on the early stages of its decomposition development fastidious and occupy all favorable places for growing: proves the success of photosynthesizing plants. rocks, hollows and corniches, places with fine clastic Accordingly, one of the adaptive characteristics of stones, beaches, etc. In particular, hair grass grows in D. antarctica and C. quitensis can be the ability to separate agglomerations or form thick cover on the absorb nitrogen on different stages of its transforma

139 140 OZHEREDOVA et al. tion. But this adaptation is not unique for Antarctic environmental temperature and launch a range of vascular plants. defense reactions, particularly the formation of free In the maritime Antarctic, D. antarctica is often fatty acids and free sugars and the synthesis of defen found in moss areas, especially Sanionia uncinata sive proteins: antifreeze, dehydrin, and chaperone (Hedw.) Loeske, which is a dominant species. At the proteins. They all are multifunctional proteins that same time, D. antarctica is able to absorb organic mat regulate processes of translation and transcription and ters from soil by 160 times faster than moss growing separate oxidation and phosphorylation during low nearby when temperature increases [14]. Plants temperature stress [23]. D. antarctica can absorb small peptides (di, tripep D. antarctica has typical biochemical adaptive tides) from soil directly by root hairs. This property mechanisms that are characteristic of plants growing gives a significant advantage to hair grass in acclima in low temperature [4]. D. antarctica and C. quitensis tion in new area but this property is typical for family can be referred to cryophytes, organisms living in low Poacae on the whole. Plants of family Caryphyllaceae temperature [25]. In general minimal photosynthesis are able to absorb minerals from interstitial water, but temperature is liquid freezing point (–1…–2°C), and root system can cause dissolving of compounds that cryophytes photosynthesize in even lower tempera are unavailable in nonsoluble form [14]. ture. Thus, for example, Pinus pumila photosynthesize ° Cold endurance. It is known that vascular plants under snow at –7 C. Antarctic lichen can photosyn thesize at –10°C [26]; as for D. antarctica, optimal include most of economic species. And they are char ° acterized by interspecies variability of cold endurance. temperature for photosynthesis is 10–12 C in natural This fact determines the thorough study of mecha conditions. For C. quitensis, this index value is not nisms of low temperature adaptation of plants that clear. Plants D. antarctica and C. quitensis endure low grow in severe climatic conditions [15, 16]. Antarctic temperature and drought as well and they are still able plants possess developed avoidance strategy. In partic to photosynthesize at the freezing point [9]. ular, this is typical for C. quitensis, since this plant General cold endurance of D. antarctica is much seems to be low clump and is mostly found near higher higher (LD50 = –26°C) than in C. quitensis (LD50 = clumps of D. antarctica or in hollows between stones –5°C) [4, 27]. avoiding direct influence of unfavorable abiotic fac One of the early reactions to cooling is oxidative tors. In some regions of the maritime Antarctic, stress, which causes disorders of enzyme activity C. quitensis is only found in some localities that are located on chloroplast and mitochondria membranes. probably the most protected from unfavorable condi Enzymes also cause the processes of oxidative and tions. photosynthetic phosphorylation. Formation of adap Besides, both plants have specific resistance or tive mechanisms of maintenance of photosynthetic endurance mechanism on the level of the whole organ activity in conditions of low temperature is realized on ism (anatomic changes). The mechanism is maintained the level of ultrastructural organization and biochem by the synthesis of some stress protein classes and also ical level of photosynthetic reactions as well [28]. We other compounds that provide for plant endurance [17, found that D. antarctica undergoes structural changes 18]. Generally, the increase of plant endurance to low in cells of leaf mesophil. Chloroplasts have irregular temperature is the complex result connected with con shape with pouches or invaginations inside of siderable rearrangement of physiological and biochem organelles and growths to enlarge the chloroplast sur ical processes and the changes of expression of a great face. This increases the productivity of photosynthe number of genes [19–22]. sis. Leaf mesophil cells of hair grass contain atypical We found that heat and cold shock cause the structures as well. They are numerous bladders of dif changes in gene activity in plant cells and other organ ferent size with concentrically located membranes. isms. Moreover, when temperature decreases, specific These formations are connected with adaptation to genes start functioning and synthesize certain pro climatic conditions of the Antarctic [29]. The data on teins. In addition to a great number of involved respective studies on C. quitensis are absent. enzymes, we isolated some families of proteins that are Earlier, it was mentioned that plants D. antarctica specifically connected with these processes. Accord and C. quitensis have different levels of cold endur ing to the scheme of Kolesnichenko et al. [23], at the ance. The difference of antifreeze activity between moment when environmental temperature decreases, these plants can reflect the realization of different the synthesis of stress separating proteins that launch strategies for freezing prevention, which are found to thermogenesis begins. Wellknown coldshock pro be successful for existence in the Antarctic [27]. Death tein 310 (CSP) separates oxidative phosphorylation, of plant cells and an organism on the whole can occur which allows the use of oxidative energy for the as ice crystals that form in intercellular space take increase of temperature in plant organs by 4–7°C water from cells causing dehydration. Simultaneously, higher than in the environment (thermogenesis) [24]. they have mechanical influence on cytoplasm damag This helps plants to maintain positive temperature for ing cell structures. Due to antifreeze proteins during some time and prepare for the further decrease of severe cold in intercellular space of D. antarctica,

CYTOLOGY AND GENETICS Vol. 49 No. 2 2015 MECHANISMS OF ANTARCTIC ADAPTATION 141 small ice crystals are formed that do not damage cells during adaptation. For dehydration of cells under [10, 29–31]. We consider that accumulation of some effects of water stress due to high hydrophilism, these antifreeze proteins is one of the main adaptive mecha proteins prevent water loss and stabilize other proteins nisms [32]. [23]. In addition, some dehydrins carry out antifreeze and cryoprotective activity simultaneously, and also We found that hair grass synthesizes antifreeze pro take part in the endurance regulation of plant cells to tein with weight of 22 kDa (see review [4]), whose one cold stress [39]. function is to hinder the process of ice formation [23]. Similar proteins are accumulated mostly in conduc We identified genes of dehydrin encoding proteins tive and cover tissues, where initial ice formation zones (with weight of 58, 57, 55, 53, 48, 30, and 27 kDa) of are usually located. The presence of antifreeze pro D. antarctica. Gene expression of D. antarctica is reg teins in D. antarctica is not occasional, since they are a ulated by low temperature, saline, and osmotic rather widespread adaptive factor of plants, which stresses. These proteins are accumulated in initial ice allows them to endure low temperature [33]. Winter formation zones. In D. antarctica, we found abscisic cereals have numerous defensive mechanisms and aciddependent and independent methods of dehy they efficiently take water from cytoplasm into apo drin regulation, but certain mechanism of acid partic plasts during cold shock, and, thus, avoid formation of ipation in the process of coldinduced gene expression ice crystals inside of cells. In particular, antifreeze pro is not clear [40]. They are probably necessary for plant teins of hair grass are able to inhibit recrystallisation of survival under effect of low temperature for long. For water in intercellular space and are encoded by gene C. quitensis genes, we did not determine dehydrin IRIPs (Ice recrystallization inhibition proteins) encoding proteins, but these plants can survive in the which, however, is not specific only for this plant spe Antarctic. C. quitensis can have other mechanisms of cies (see review [4]). According to our findings in the survival in conditions of low temperature for long, but database NCBI [34], the group of proteins IROPs explanation of these mechanisms needs further study include seven different proteins. Besides, we found the ing (see review [4]). presence of two more proteins that emerge in response Kolesnichenko et al. [23] conducted the compara to low temperature (cold). Their attachment to IRIPs tive analysis of six varieties of L. with is not explained. The difference for the mentioned Medicago sativa contrastive frost endurance, which showed that two gene, which is typical for different species, possibly, is mRNA— and —are accumulated dur that antifreeze protein gene expression occurs in most MsaciA MsaciB ing cold acclimatization. They encode proteins that plants during low temperature acclimatization or contain glycerinrich motives. This confirms that the hardening. At the same time, we found IRIPactivity ability to accumulate proteins similar to MsaciA and in hair grass leaves of unacclimatized plant [35], but it MsaciB to a high level can be connected with plant was not confirmed during usage of other analysis endurance to low temperature. Regarding both Ant method [36]. arctic vascular plants, the data on proteins similar to We conducted the search of sequences (as nucle those mentioned above are absent in the literature. otides as amino acids) of in the public spe C. quitensis Most stress proteins are chaperones synthesized de cialized databases and it showed that, currently, there novo, whose number sharply increases under effect of are only seven nucleotide sequences of (for C. quitensis stress factors. Numerous functions of proteins of this two of them, we established or verified attributes, and family are determined by their chaperone activity. In five are not checked). But none of them is homologous particular, they are involved in the processes of regular to hair grass gene IRIPs [34]. Verified sequences con noncovalent arrangement of polypeptides or struc cern complete sequence of retrotransposon Cassandra tures with polypeptides that are not components of TRIM [37] and sequence of gene 18S of ribosome newly formed structures. It is considered that molecu RNA, ITS1section of gene 5,8S of ribosome RNA, lar chaperone, except for joining and stabilization of and ITS2section of gene 28S of ribosome DNA. other proteins that are unstable in certain conforma Unverified chloroplast sequences are partial sequence tion conditions, contribute to acquiring of cell endur of Ksimilar gene, partial sequence of gene tRNALeu ance, since they take part in accompanying, oligomer ( ), complete sequence of intergenic wedge trnL trnL ous assembly, and transportation into certain subcellu and partial sequence of gene ( ), par trnF tRNAPhe trnF lar protein compartments or release of them by means tial sequence of genes ( ) and ( ), PsbZ psbZ tRNAGly trnG of the denaturation method [39]. These hydrophil partial sequences of intergenic wedge and trnQrps16 proteins are formed in cytoplasm under effect of low gene S16 of ribosome protein ( ), and partial rps16 and high temperatures and accumulate in cell walls. sequence similar to dehydrogenase gene NADH of We showed that accumulation in wall cell occurs in subunit F [38]. Thus, the problem of pearlworts' adap after temperature stress. This protein has tive system needs further studying. D. antarctica molecular weight of 70 kDa [6]. It helps to transform Dehydration and dehydrins. Low temperature stress aggregated or irregularly convolute proteins into solu is closely connected with cell dehydration and tion and vice versa using some cycles of attachment enhanced dehydrin synthesis is characteristic of plants and hydrolysis of adenosine triphosphate [41].

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Thus, we can assume that this protein ensures low nisms of plants under effect of stress factors, adapta temperature photosynthesis optimum (+12°C) (see tion, and homeostatic character on the level of sepa [4, 6]). To conclude, D. antarctica realizes the method rate organism. Plant genome plasticity substantiates of synthesis of stress proteins typical for other vascular totipotency (switching of morphogenetic programs, plants, which provide for photosynthetic activity in for example, with the purpose of restoring of damaged temperature stress conditions. Also, D. antarctica is an organs or organism on the whole) and regulated important component of defensive reaction of live (adaptive) changeability of genome in ontogenesis organisms in response to effect of unfavorable abiotic (including emergence of genotrophs), and also high factors. Respective data concerning C. quitensis are frequency of, prima facie, undirected genome changes absent in the literature. under the effect of different environmental factors One more defensive mechanism of plants to low [48–50]. temperature for a period is accumulation of soluble According to the data given in the review [4], sugars in tissues. Thus, maximum accumulation of D. antarctica is characterized by karyotype 2n = 2x = 26, saccharose, fructose and glucose in D. antarctica leaf with formula 10 m + 6 cm + 8 st + 2 t. Chromosome tissues is observed before Antarctic winter [42, 43]. number 2 n = 26 with main number x = 13 is generally Some scientists studied expression of gene encoding typical for species of genus Deschampsia. And only two saccharose phosphatesynthetase enzyme of D. antarc species have the main number of chromosomes of 7— tica. We discovered that the activity of mentioned D. atropurpurea (2 n = 14) and D. flexulosa (2 n = 28), enzyme increases in response to low temperature, but which belong to separate genera according to the data number and level of proper encoding gene expression of molecular taxonomy. We used the methods of does not change [44]. Cbanding, analysis of restriction spectra of plastid Resistance to ultraviolet radiation. D. antarctica and nuclear DNA, and isozyme spectrum to deter and C. quitensis are well adapted to UV radiation. mine the difference between D. core, D. atropurpurea Thus, under effect of UVΒ, the leaves of these plants and D. flexuosa. C. quitensis has chromosome set 2n become smaller and shorter but thicker. We can with 80 chromosomes. Because of small size of chro observe the increased content of photosynthetic pig mosomes, the complete study of karyotype was not ments there. The life span of C. quitensis leaves conducted. At the same time, karyotype with such becomes shorter. UVΒ radiation accelerates ripening number of chromosomes is determined for close spe and favors the increase of a number of blossom cluster cies C. apetalus and C. affinus. and fruit. UVΒ radiation does not influence the life There are data on the presence of aneuploidy cells span of seeds [45]. In the experiment, we compared in meristem of some plants and even particular aneup plants D. antarctica that grew in natural and hothouse loidy plants D. antarctica. The studies of appendage conditions (without UV influence) and found that, in roots of D. antarctica from the islands of Galindez, natural conditions, D. antarctica had 50% less output of Piterman and Barselot (area of Akademik Vernadsky total vegetative biomass in comparison with hothouse Ukrainian Antarctic Station, maritime Antarctic) plants and 47% less than land biomass. The decrease of proved our findings. Besides, we discovered mixop land biomass growth was the result of the decrease of loidy (polysomaty) of this species. Also number of leaf extension speed (grew shorter leaves) by 29% and chromosomes in cells of meristem of root tip is signif the decrease of general leaf area by 59% [46]. icant—from 10 to 68 chromosomes [51]. Thus, It is known that pcoumaric, caffeic, and ferulic D. antarctica of this region does not demonstrate mix acids are predecessors of hydroxycinnamic acid and oploidy regarding a number of chromosomes com lutein derivatives, which are dominating flavonoids pared with generic number and it is characterized by both in insoluble and soluble extracts from leaves. the presence of aneuploidy. Concentrations in insoluble pcoumaric and caffeic Species formation inside of the genus irrespective acids and soluble ferulic acid in D. antarctica in condi Β of areal (and, in most cases, specimens of genus Des tions of natural UV radiation are higher in compar champsia are adapted to conditions of cold humid ison with hothouse conditions by 38, 48, and 60% cor meadows) is not accompanied with the change of respondingly. This means that flavonoids formed chromosome number. Except for diploid sets, some under UV radiation effect can protect cellular struc species are characterized by polyploidization and ane tures from damages [46]. This reaction of D. antarctica uploidization. Karyological variations of species of is neither speciesspecific [17]. Plants C. quitensis have genus Deschampsia, particularly D. caspitosa, are photoprotecting properties that can be referred to caused by fusion of smaller chromosomes with further effect of flavonoids and carotinoids and act as UV polyploidization. This process is rather widespread absorbing molecules and antioxidants [47]. among plants [52]. We found features of eco Plasticity of genome in extreme living conditions. logical differentiation connected with the level of High plasticity of genome of somatic cells becomes plant ploidy. At the same time, diploid plants had apparent in ontogenesis and is formed on the basis of lower indices of realization of potential ecological wellknown cellular and molecular defensive mecha niche than polyploid ones. The level of such realiza

CYTOLOGY AND GENETICS Vol. 49 No. 2 2015 MECHANISMS OF ANTARCTIC VASCULAR PLANT ADAPTATION 143 tion and ploidy increased [53]. Probably, such a ten and reasons of phenomena described by other authors. dency is the basis for creation of species forms with tet They connect the established aneusomatic character raploid (n = 13) karyotype, for example, D. obensis, D. with influence of different environmental factors, par mackenziana, and D. mildbraedii. In general, we found ticularly temperature. But similar data on C. quitensis that polyploidization can cause separation of endemic is absent in the literature. forms in specific conditions of increase [54–57]. There is no data on aneuploidy in C. quitensis in the lit erature. CONCLUSIONS We also conducted cytological analysis of D. cae The comparative analysis of adaptive mechanisms spitosa from populations of the northern part of Lake of native Antarctic plants Deschampsia antarctica and Ontario (Canada), which proved the presence of ane Colobanthus quitensis to severe environmental condi uploids and variation of diploid number of chromo tions demonstrates a range of generally accepted somes from 18 to 26. Besides, specimens with 2 n = 26 adaptation ways owing to basic genetic plasticity, have additional or socalled Βchromosomes. The role which do not distinguish the given species between of Βchromosomes, which were also detected in other vascular plants. Despite the difference in adap D. wibeliana, is not discussed [58]. However, scientists tive strategies of these species, they are generally recently consider that Βchromosomes maintain equally adaptive. The reasons why perlworts are not endurance of many species of organisms in unfavor rather spread, are not probably connected with basic able natural conditions. Certainly, Βchromosomes adaptive mechanisms but survival methods for this appear resulting in main chromosome changeability species and habitation in particular regions in the past and can influence adaptive plant potential, which historical epochs. becomes apparent not only by particular changes of Β plant phenotype with chromosomes but also with REFERENCES the increase of genome changeability level. This increases plant population polymorphism by unfavor 1. Voinikov, V.K., Borovskii, G.B., Kolesnichenko, A.V., able conditions of habitat [56]. By the way, Βchromo and Rikhvanov, E.G., Stressovye belki rastenii (Stress somes have been recently discovered in D. antarctica Proteins of Plants), Irkutsk: Inst. Geogr., Sib. Otd., that grow on the Darboux Island (unpublished results Ross. Akad. 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