Towards angiosperms genome evolution in time

In this communication, direction of evolutionary variability of parameters of genome size and structurally functional activity of plants in angiosperm taxa among life forms, are analyzed. It is shown that, in the Cretaceous–Cenozoic era, the nuclear genome of the plants tended to increase. Functional genome efficiency (intensity of functions per pg of DNA) decreased as much as possible from highest, at trees and lianas of rain and monsoonal forests of the Paleogene, to minimum, at shrubs, perennial and annual grasses of meadow–steppe vegetation appeared in the Neogene. Environmental changes in temperature, humidity and CO2 concentration in adverse direction, critical for vegetation, are discussed as the cause of growth of evolutionary genome size and loss in its functional efficiency. The growth of the genome in the Cenozoic did not lead to the intensification of functions, but rather led to the expansion of the adaptive capacity of species. Growth of nuclear DNA content can be considered as one of the effective tools of an adaptogenesis. INTRODUCTION Nuclear DNA content (nDNAc) in plant and animal cells is being investigated for more than 50 years (Bennett and Leitch, 2005a); and so far, the nDNAc has been defined for 6.5 thousand angiosperm species. This information is summarized in tabular forms in several publications (Bennett, 1972; Bennett and Smith, 1976, 1991; Bennett et al., 1982, 1998, 2000; Bennett and Leitch, 1995, 1997, 2005a; Hanson et al., 2001a, b; Hanson et al., 2003, 2005; Suda et al., 2003; Zonneveld et al., 2005) and in free online database (Bennett and Leitch, 2005b). We enlarged this database by adding more information about geological age of plant genera (after Daghlian, 1981; Muller, 1981; Zavada and Benson, 1987; Benton, 1993; Collinson et al., 1993; Herendeen and Crane, 1995; Wing and Boucher, 1998; Crepet et al., 2004; Song Zhi–Chen et al., 2004; Martínez–Millán, 2010; Grimsson et al., 2011 and The Paleobiology Database (PBDB – http://flatpebble.nceas.ucsb.edu/cgi–bin/bridge.pl)) and their growth forms. This research is undertaken to detect changes in nDNAc, number of chromosomes, ploidy levels in angiosperms and their taxonomical subunits and different growth forms, during the course of evolution from late Cretaceous to Plio–Pleistocene. Influence on dynamics of the climatic factors as well synchronism with changes of structurally functional characteristics of 1 Corresponding author. E-mail: Serge Sheremet’ev, [email protected] plants is studied. On possibility of such coordination point the known facts of influence on a wide range of properties of plant nDNAc is documented (Grime, 1998; Reeves et al., 1998; Prokopowich et al., 2003; Jovtcheva et al., 2006; Beaulieu et al., 2007a, b; Beaulieu et al., 2008; Knight and Beaulieu, 2008 и др.). Being engaged in this work, we understood nevertheless some vagueness of such constructions about the assumption what data obtained from extant species has remained unchanged over geological time. This assumption is quite vulnerable relative to ploidy levels, to a lesser extent – relative to the numbers of chromosomes and the amount of DNA content in haploid sets of chromosomes. However this question, in our opinion, is interesting and demands the preliminary analysis and discussion at least. We offer the certain probabilistic approach which correctness can be estimated by the general logic of angiosperms evolution, and also by coincidence of the received curves with climatic data. However, it should be noted that there are different approaches to this problem (Masterson, 1994; Franks et al., 2012). We dare to hope that in the future, these approaches would supplement each other. DATA SETS In addition to above mentioned data, following data sets were also used: cell cycle time (Francis et al., 2008), leaf functional traits Amax (photosynthetic capacity, per leaf dry mass) and SLA (specific leaf area, per leaf dry mass) (Wright et al., 2004), leaf vein density (Brodribb and Field, 2010; Feild et al., 2011), plant water relations (index of plant water relations complexity and partial volume of intercellular spaces) (Sheremet’ev, 2005), and chlorophyll content (per leaf dry mass) (Lubimenko, 1916), oxygen isotope ratio in shells of planktonic foraminifera and brachiopods from J. Veizer’s database (http://www.science.uottawa.ca/geology/isotope_data/) (Veizer et al., 1999), arid areas (computed after paleomaps by Scotese, 2003; Akhmetiev, 2004; Chumakov, 2004a). All data were averaged by epochs (Ogg et al., 2008). TERMINOLOGY The labeling of nDNAc is done by the use of the term "C–value" with various prefixes – 1С, 2С, 3С etc. It was used for the first time by Swift (Swift, 1950) without any definition. Later Bennett and Smith (1976) pointed out, that Swift in personal communication informed that the letter C stands for 'constant', i.e. the amount of DNA characteristic of a particular genotype. They defined the C–value (or 1C value) for any genotype as the DNA content of the unreplicated haploid chromosome complement (Bennett and Smith, 1976). Similarly, the measure of DNA content of unreplicated non–reduced (zygotic, diplophasic) complements will be 2C (irrespective to ploidy level) (Greilhuber et al., 2005). Unlike the term "C–value" the term “genome size” is often used to designate the quantity of DNA in meiotic reduced diploid set of chromosomes or monoploid one (meaning the polyploid set contains more that one genome) (Bennett et al., 1998). Consistent use of the term "genome size" in a narrow sense is often impossible due to uncertainty of the degree of ploidy. Therefore many authors prefer to use this term, as well as "C–value" in a broader sense irrespective of the ploidy level. In this sense, the terms "C–value" (with prefix 1) and "genome size" are synonymous (Greilhuber et al., 2005). The complete chromosome set with number n (reduced) irrespective of the degree of generative polyploidy was offered the term "holoploid genome" (Greilhuber et al., 2005; Greilhuber and Doležel, 2009). It was proposed to use the terms "holoploid genome size" and "C–value" (or 1C) to determine size of genome (Greilhuber et al., 2005). In that case 2C will be related to an unreplicated, unreduced chromosome set (2n) regardless the degree of ploidy and will characterize total amount of the nuclear DNA (in diplophase), and the genome size will correspond to the term "holoploid genome size" (or 1C). In this article, we will hold these definitions for these terms. VARIABILITY OF TRAITS Traits that characterize nuclear DNA of angiosperms (2C, the number of chromosomes and ploidy level) vary at broad limits. Especially it concerns the nDNAc whose coefficient of variation is more than 150 % (Table 1). More moderate variations are discovered in chromosome numbers (71%) and ploidy levels (59%). The wide variation of genome size in flowering plants (from 0.05 to 140 pg) is a part of greater variety of 1С among eukaryotic organisms – from 0.009 to 700 pg (see, for example: Leitch et al., 1998; Gregory, 2005; Patrushev and Minkevich, 2006, 2007). This variation, which is not related with the taxonomic positions of the species and their phenotypic complexity, was called the "C–value paradox" (Thomas, 1971). However, the fractile analysis shows that the variability of the data is not so considerable (Table 2). The difference of the nDNAc between the top and bottom deciles (fractiles 0.9 and 0.1 respectively) makes only 32.3 pg. In other words, the vast majority of array values (80%) are in limits of 1.2–33.5 pg. By such consideration the genome sizes are limited at a range of 0.6–16.7 pg; when, number of the chromosomes changes from 14 to 48, the ploidy levels do not exceed 4 (Table 2). Comparison of these data with the variability which is shown in T ab le 1 . N uc le ar D N A c on te nt (2 C , p g) , n um be r o f c hr om os om es (2 n) a nd p lo id y le ve ls (P L) in d iff er en t g ro w th fo rm s o f a ng io sp er m s St at is tic s A ng io sp er m s M on oc ot s D ic ot s