A New Alternative for Plant Breeding, Biodiversity and Environmental Sustainability: Apomictics
Aim of this study is to explain of the apomixes, utilization
in the plant breeding and to indicate its importance in terms of biodiversity
and environmental sustainability. Etymologically, apomixis comes from
the Greek apo (= away from) and mixis (= act of mixing). Botanically,
apomixis is a kind of biological reproduction process without fertilization
and meiotic division. These types of plants produce with genetically identical
seeds to their female parent. It is uncommon in the wild and rare in cultivated
crops. If it is possible to exploit or harness this type of reproduction,
then produce new cultivars more quickly and cheaply. Similarly, the breeding
process will be significantly accelerated in related seed companies, furthermore,
farmers and growers would be able to reduce costs in their production
input/s in terms of, for example, the purchase of hybrid seed, time saving
and the size of labor force, etc. or reach a maximum yield potential level.
In spite of the many potential advantages, according to some researchers
the development of commercial apomictics is making slow progress. However,
other research from a multidisciplinary approach to apomictics indicates
that all potential obstacles could be overcome in commercial production
in the near future. With this contribution, thousand million persons who
dye from hungry could be saved and their basic and vital requirements
could be met.
Apomixis is a natural process that allows clonal propagation by seed, resulting in off-spring that is genetically identical to the mother plant and if can be exploite, this process will be a new milestone and the beginning of a new era for plant breeding (Adolfsson and Bengtsson, 2007) and seed production, since it allows the immediate fixation of desired genotype, including F1 hybrids without any segregation in off-springs (Anonymous, 1994; Grossniklaus et al., 1998; Ulukan, 2007). In nature, apomixis is widespread but infrequent biological phenomenon. It occurs in arround 10% of the 400 families of flowering plants, but only in 1% of the 40,000 species that make up those families. Many wild plants and some families such as Alliaceae, Apiaceae, Asterceae, Brassicaceae, Compositae, Orchidaceae, Plumbaginaceae, Rosaceae, Rutaceae, Solanaceae, Urticaceae and certain tropical forage grasses have apomictic plant species (Ramulu et al., 1999; Spillane et al., 2001; Kaushal et al., 2004; Ozias-Akins and van Dijk, 2007). According to Ozias-Akins (2006) apomictics (only) preserve the maternal genotype by parthenogenetic embryo development so they maintain their heterozygosity and epistasis and they produced by cloned seed and enable them to reproduce asexually (Dresselhaus and Colombo, 2001) with their viable pollens. Plant breeders are very interested in their advantage(s) in terms of propagation and reproduction of them and this issue will be discussed later. On the one hand, apomixis pecularity could also be transmitted through the more common mechanism of sexual reproduction. Generally, this phenomenon does not occur naturally but there are some exceptions such as some citrus fruits (Citrus spp.), major field crops [rice (Oryza spp.), wheat (Triticum spp.), rye (Secale spp.) barley (Hordeum spp.)]. On the other hand, apomictic relatives that can be crossed with eachother. Furthermore, commercial hybrid production systems are available and this has made a major impact through the simplification of the hybrid seed production (Şehirali and Özgen, 2007) in some important field crops such as maize (Zea mays L.), sorghum (Sorghum spp.) and millet (Pennisetum glaucum (L).R.Br.). According to study results, the increase in yield with the fixation of hybrid vigor of inbred crops such as wheat (Triticum spp.) and rice (Oryza spp.) by apomixis was observed to be 15.0 and 35.0%, respectively (Asker and Jerling, 1992). The aim of this article is to make general evaluation on the usage possibility (ies)-exploitation (s) of the apomictics in the plant breeding, their impacts on biodiversity and environment and to make some recommendations and suggestions on breeding and seed production processes, biologically.
Reproduction modes in the plants (Modified from Spillane et
al., 2001; Şehirali and Özgen, 2007)
Seed development occurring without fertilization is called apomixis and occurs
naturally in some crop plants (Fig. 1) (Van Dijk and Van Damme,
2000; Şehirali and Özgen, 2007) and it is mainly seen in polyploid
plants, because it was the apomictic mutants that survived in the course of
evolution (Kumar, 2006). Scientists have classified this phenomenon into two
basic sub-classes according to whether unreduced cells give rise to a mega-gametophyte
(= gametophytic) or to an embryo (= sporophytic) and the usefulness in the plant
breeding (Spillane et al., 2001; Kaushal et al., 2004; Ozias-Akins,
2006). In spite of the fact that apomoxis eliminates practically all of the
potentially negative processes associated with sexual reproduction, adventitious
embryony retains an important physiological characteristic of the sexual process
and other types of agamo-spermy which is the ability to produce the distinctive
characteristics of the seedling. To identify the apomictics by determing the
location of the gene, researchers are using many advanced recognition and characterization
biological tests and techniques such as cyto-embryological/cytological or histological
tools, some DNA-Molecular Markers (RFLP, RAPD, AFLP, SSR, etc.) (Estrada-Luna
et al., 2002; Ozias-Akins, 2006). Genetic studies on the apomictic mechanisms
are difficult to conduct and frequently they reach a dead end because of the
lack of the necessary crosses and backcrosses for the tests on the segregated
progenies. Similarly, if the plants reproduced by facultative apomixis, it is
difficult to understand the inheritance of them (Hanna, 1995) thus, apomixis
controlled genes have not yet been found in major cultivated plants (especially
in the Poaceae family). However, these genes can probably be found in wild species
or related crop cultivars. As a result of the study, it was understood that
apomixiss heritage pathway was under the control of qualitative inheritance.
This point is very clear and progress is being made in understanding the genetic
control of apomixis in various cultivated plants (Ozias-Akins, 2006; Ozias-Akins
and van Dijk, 2007). The simple structure of the genetic control of the apomixis
makes it easy to improve the potential for manipulating the reproductive mechanism
and transferring it to other plants. In terms of this aspect, certain successful
examples were obtained in Brachiaria spp., Eragrostis spp., Panicum
spp., Paspalum spp., Pennisetum spp. and Tripsacum
spp. (Kaushal et al., 2004). Developments in advanced biological molecular
marker techniques/tools and technological facilities had been achieved to transfer
desirable apomixis genes into non-apomictics. Similarly, use of mutagenic agents,
for example Ethyl Methanessulfonate (EMS) (Şehirali and Özgen, 2007),
may be another valuable source for the production of mutant genes for apomictic
reproduction. Parthenogenesis, apospory and other types of apomixis reproduction
have been considered by some scientists as weird (Dresselhaus and Colombo, 2001;
Adolfsson and Bengtsson, 2007). Whatever it is, development of apomictic plant
reproduction will give or reproduce stable apomictic cultivars releases for
the farmer(s)/grower(s) in a big possibility. If pseudogamous diploid progeny
can be induced in large numbers as complex hybrids; true breeding homozygotes
will easily be produced, thus, long processes for fixing the valuable new combinations
obtained from intra or inter varietal hybridizations could be eliminated. However,
to be able to understand and explain the appearance of apomixis in cultivated
plants, three factors must be defined clearly, namely they are hybridization,
polyploidy and related genetic factors.
MATERIALS AND METHODS
This study was carried out at the Department of Field Crops, Faculty of Agriculture,
University of Ankara, during 2009, Ankara, Turkey. The development of apomixis
in the plants has two important effects in terms of evolution. First, a species
group gives rise to innumerable microspecies or clonal species through the perpetuation
by apomixis of sexually sterile hybrid derivatives, the genetic and morphological
barriers between the male and female parents (Asker and Jerling, 1992); second
the genetic analysis of them provides to researchers certain handicaps because
of their ploidy levels, lack of sexual progeny, lethality, accurate identification
and classification of the progeny. According, to the simple inheritance hypothesis,
one or two dominant genes control apomixis (Asker and Jerling, 1992). And it
is well fitted in the Mendelian segregation ratio (1:1) for apomictic plants
in sexual progenies that are hybridized from sexual and apomictics reproduction.
When the apomixis, governed by a dominant gene or a simple inheritance pathway
in the plants, all are heterozygous for their reproduction and their usage is
very easy in the plant breeding programs. (Sexualxapomictic) hybridizations
result in both sexual and apomictic F1 genotypes and one half of
the F1 plants are sexual and the reminder are apomictics. Afterwards,
all plants obtained from one half of the sexual F1 plants can be
discarded or used in hybridizations with other apomictics to produce new (apomictic)
hybrids and sexual plants with the new gene combination. Furthermore, by using
sexual plants in the crosses with improved apomictics from other hybrids in
each generation, the possibility of developing superior apomictic hybrids increases
in advanced generations. So, F1 apomicts with desired biological
and agronomic trait(s) produced from the hybrid can be selected and they can
be re-used as desired in any kind of breeding programs. Moreover, at the end
of these procedures, doing progeny and stability tests for these genotypes is
not necessary to understand if they are obligate apomictic or not and the obtained
superior genotypes can be released as cultivars. These released cultivars are
apomictic hybrids (either in terms of F1 and or subsequent generations)
under related conditions. On the other hand, if the apomixis phenomenon is controlled
by a recessive gene, all F1 sexual plants will be heterozygous in
hybrids between sexual plants and apomictics. Thus, the breeding strategy will
change in process of time. If the inheritance pathway works in the way mentioned
above, breeding procedures will be rather complex and they can change according
to the particular plants (or parents and hybrids), their genetic background
and effective gene numbers. In any commercial plant breeding program, if a male
sterile line use for the apomictic undesired apomictic traits can be easily
eliminate from those materials (male sterile A, male fertile B, maintainer lines,
R-lines etc.) to develop the quality and quantity. Generally, the main trend
is to determine or select the superior apomicts cultivar release (Stebbins,
1941) in the hybrid populations after that stage as candidates besides certain
cytological, biological-biochemical, histological, histo-chemical and advanced
tests. Unfortunately, despite all efforts, no clear apomixis gene(s) has/have
been clearly identified or isolated or successful transferred to the cultivated
plants, furthermore it may vary, except for some minor successful attempts at
the academical level within the same genus.
AS AN EFFICIENT TOOL IN THE PLANT BREEDING
There are three types of breeding approaches in apomixis:
(transfer of the apomictic genes from wild relatives by interspecific
biology and genetic engineering techniques (Kaushal et al., 2004)
And basically there are three main and important plant breeding methods (mutation
breeding, selection and backcrossing and cloning) are valued for apomictics
(Fig. 2) and the remainder techniques are combinations of
these methods (Ulukan, 2009a). It is clear that many angiosperms but apomictic
plants exhibit genetic variation (Adolfsson and Bengtsson, 2007) in terms of
sexual versus apomictic seed production, but there are few scientific findings
on the extent of this in natural populations (OConnel and Eckert, 1999).
They are produced through seed, but their embryos are developed from the cells
in the ovary without fertilization; so they are genetically similar to their
mothers. During this stage, mutation breeding technique has an important place.
As known, mutation agent applications have pleiotrophic effects because they
turn on the genes that normally remain re-pressed, including those epigenetically/silenced
via DNA methylation (Kumar, 2006).
chart for the apomictic breeding methods (Modified from Bashaw, 1980;
Şehirali and Özgen, 2007).
So, this method (mutagen agent application(s)) is used for developing a new
cultivar from the wild forms, cultivar(s) and population(s); after selecting
according to desirable characters phenotypically. But, in some plants, for example
Kentucky bluegrass, (Poa pratensis L.) the apomixis trait is optional
and apomictic seed amount is equal to the sexually produced amount. Likewise,
the sexuality degree only varied between 1-50% or more in them. In addition,
obtained research findings showed that, sexuality degrees could be affected
from the internal factors such as the plant age and some external factors (temperature,
water, light, time, etc.). So, a plant species can be totally apomictic in an
environment but may not be in another environment. Nevertheless, to be able
to find and maintenance apomictic plant species is possible if these breeding
methods are used properly (Fig. 2). It is well known that
apomictic plants produce through seed but they do not have insemination. So,
they do not show any segregation in their off-spring.
Agricultural scientists would dearly love to convert these plants to apomixis:
making embryos that are genetic clones of themselves rather than the product
of sexual reproduction with its inevitable gene reshuffling and after 20 years
of study, an apomictic corn (maize) has been produced, but it does not yet produce
enough viable kernels to be useful commercially. Basic aim of the plant breeding
which will be carried out for the apomictics is to obtain genetic recombinations
and identify them among the progenies as superior/true-breeding apomictics at
the level of suitable cultivar status. For this, obligate apomictics can only
be used as male parent (they are genetically recombined and comprise chromosomally
reduced male gametes) in all kind of plant breeding programs and they are generally
called gorgeous and opportunist due to the remarkable polymorphism of the complexes,
also being considered as heterotic, aggressive (frequently) and competitive
(Bashaw, 1980). However, these plants (apomictics) are adapted to flora and
they have taken great advantage of conditions and they have adjusted themselves
to changes in the biotic and abiotic stress factors over a long period. This
phenomenon usually happens in the polyploid plants and it may be necessary at
the level of tetraploidy or higher levels (Ramulu et al., 1999); but,
they have been most valuable genetic tools for the plant breeders in the 21st
century (Asker and Jerling, 1992). In addition, cultivating apomictic plants
would reduce the costs of hybrid production and it would be possible to produce
virus-free plants, particularly in Citrus (Citrus spp.) crop plants.
This trait will allow to breeders to create perfect and precisely engineered
plants which combine agronomically desired traits in one genotype (Ramulu et
al., 1999; Ulukan, 2009a, b). Producing by apomixis to determine the hybrid
seeds could lead to impressive time and cost savings. Some attempts were made
to produce apomictic cereals but with very limited success and generally, no
apomictic cereal cultivars has/have been released up to now. As mentioned above,
it can be said that these topics still wait for a successful solution (Kaushal
et al., 2004). According to research results, it is estimated that with
the introduction of apomixis trait to the rice (Oryza spp.) crop plants
the total annual gain will be US$ 2.5 billion in the world (Grossniklaus et
al., 1998). The implications of the apomixis-led acceleration of the plant
breeding could be dramatic; lower costs and much reduced time requirements will
change the face of the plant breeding and related sectors and farmers or growers.
Similarly, if apomixis and plant genomics can also be combined, rapid and uniform
delivery of quality crops to the products end-users in terms of food,
fibre, pharmaceuticals, plastic or as raw material will be possible. If public
attention is drawn to this topic, it will likely result in a general decrease
of seed and seedling prices. But, one or a few seed/seed(ling) companies controls
the apomixis, their potential effects will be disseminated immediately, directly
or indirectly. However, poor farmers in developing countries, could be negatively
affected in two ways, firstly, they could not use and secondly they could save
these seeds (Dresselhaus and Colombo, 2001). It is not necessary to wait for
rich farmers longer to be able to get or access new hybrid seed for every growing
season in order to ensure sufficient agricultural production. This point is
particularly very important in undeveloped countries. The apomixis phenomenon
may increase access of farmers to hybrid seeds, but can not let them take the
control of the seeds. These farmers have to learn how to obtain faster breeding
procedures, to take control of their local agro-environment conditions and to
obtain cheaper seed of more adapted varieties for their production. This is
wholly possible and depends on whether apomixes is accessible to those who want
to use it. In addition, the superiority of vegetative reproduction by seed has
a major impact not only on vegetatively reproduced but also on seed-propagated
(generatively) crops and in terms of avoiding of phyto-sanitary threats in unfavorable
seasons or conditions (Ramulu et al., 1999).
AS A GUIDE TOOL IN THE BIODIVERSITY AND ENVIRONMENTAL SUSTAINABILITY
to their hybrid vigor power, all apomictics have the potential of maximizing
the crop production as food (dry matter), forage and fiber yield through
the fixation of hybrid vigor (Ramulu et al., 1999)
rapid generation and multiplication of superior forms through seed, the
reduction in cost, time and labor force for the plant breeding
avoidance of complications in sexual reproduction, not requiring pollinators,
pollination and cross-compatibility and the avoidance of viral transfer
in plants especially in vegetatively propagated plants (Bicknell and Koltunow,
the usage possibility (ies) of wild relatives could be directly integrated
into the plant breeding programmes. In apomixis technology, fixation of
any desired genotype with a certain propagation type is possible (Spillane
et al., 2001)
genotype of every apomictic is fixed in the F1 generation and
each one is derived from a cross has a potential of being the cultivar
and maintenance of their elite genotypes is easy and efficient and there
is no need for isolation criteria to produce high quality seed or seedling
main advantage of apomixis over sexual reproduction is the possibility
of selecting individual plants with the superior characteristics, propagating
them clonally by seeds and sowing true breeding seeds in crops such as
potato (Solanum tuberosum L.) (Ramulu et al., 1999)
propagation by apomixis will greatly reduce storage and transport expenditures,
losses, disease-virus spreading risks, shipping and planting costs especially
for the farmers and growers
yielded varieties is the improvement and enrichment of the security of
food supply and makes greater autonomy for specific environments in developing
countries (Bicknell and Koltunow, 2004)
Due to the fact that genetic and biological bases are still little understood
(Mogie, 1992) and not clear, its impacts on the biodiversity are open to speculation,
even contradictory to some degree. Use of the apomictics for cultivar development
in any plant breeding programme would increase genetic diversity. The introduction
of apomixis into crops plants (especially to the field crops) will alter
the genetic diversity of both cultivated forms, their wild and non-apomictic
relatives. At this point, some researchers have different opinion that the low
rate of apomixis in nature might be the result of extinction brought about by
its long-term disadvantages (Dresselhaus and Colombo, 2001). According to the
research, there is another danger for apomictics in that they can be damaged
by the natural selection process and biodiversifiying. Environmental conditions
are able to negatively influence apomictic expression in some plants (especially
under stress conditions). Similarly, sudden environmental changes, new pests
or diseases have a negative impact, as well. But, despite of all these negativeness,
apomictics have wider ecological survival range and their tolerance ability
to stress factors than their sexual diploids because they have larger and wider
distribution area. Furthermore, although it is not clear this survival may be
related to the ability to escape from predators and pests; greater colonizing
ability and the fact that often hybrids have greater genetic variability. Positive
and negative impacts can be grouped as follows (Asker and Jerling, 1992; Ramulu
et al., 1999; Dijk and van Damme, 2000; Estrada-Luna et al., 2002;
Adolfsson and Bengtsson, 2007; Şehirali and Özgen, 2007; Ulukan, 2008,
apomictic plant derived from the hybridization (sexualsxapomictics) is
potentially a unique cultivar or a hopeful candidate regardless of heterozigosity
or homozygosity genetic background of the parents
the genes which was/were responsible for the apomixes introduced into
a sexual species, all germplasms within a species have a potential as
a parent of a new hybrid and this was determined as F1, too
maintenance of elite genotypes is easy and efficient, so there is no need
for isolation criteria to produce a high quality of seed
planting of true breeding seeds from the apomictic reproduction has many
advantages over the tuber propagated crops
will reduce the spread and transition possibility of diseases and viruses
by propagated especially by tubers
reproduction by passing all of their genes to offspring has some benefits
in stable environments; but not in unstable environments and they pass
half their genes to off-spring but produce more off-spring at a lower
average energy cost and do not have to depend on neighbors or wind or
insects for pollination and do not contract sexually Transmitted Diseases
produce no wasted offspring with biologically bad or risky genes
reproduction causes variation (Adolfsson and Bengtsson, 2007; Ulukan,
2009a) and produces seeds, asexual reproduction has rapid reproductive
rate and off-spring are not as fragile as seedlings
propagation by apomixes reduces the storage, shipping and planting costs
number of apomictic genotypes can be mixed together in various combinations
to enhance genetic diversity to accomplish a specific goal
is a very complex trait, but it is governed by genes that behave individually.
So, these genes have the negative effect on the fitness, community and
the apomixis segregations or inheritance pathway can be changed (particularly
at the plant base). According to studies, intermediate parhtenocarpic
apomictics have deleterious effect owing to slow but harmful mutations
which accumulate in their structures
has biologically useful genes which can be functioned in a particular
variability is extremely low in the populations in asexual propagation
natural apomictics are triploid and their meiotic division are rather
unbalanced in the flowers, so the males are sterile
carry potential risks which differ for each apomictics. Compared with
other transgenes, apomixis transgenes have endogenous effect for uncontrollable
physiologic reactions, meiotic division etc. and demographically dissemination
superior cultivars will occupy most of the fields covered with a particular
crop using apomixis in plant breeding. These fields will be more uniform
than monocultural applications, but these cultivars will be more fragile
and susceptible to pests and diseases
is a danger for the apomixis mechanism spreading to wild populations and
the impact on genetic diversity, environment, biodiversity and plant evolution
is limited to polyploid species, which are relatively few in number in
it becomes feasible to transfer an apomixis supergenes into wild diploid
plants, they can be easily be created
competitive advantages may be affected by genetic erosion this is valid
for many wild and non apomictic relatives
of the important threats to the farmers is the potential use of Terminator
to Traitor Technologies or Technology Protection System (TPS)
RESULTS AND DISCUSSION
Apomixis is currently receiving increasing attention from the scientific and industrial sectors and it is an excellent material for experiments on the effect of the environment on the genotype and natural selection. On the basis of apomictic populations, the relative ages of different flora(s) can be estimated. Those which are young have a large proportion of apomicts, while the olders specimens have the sexual members with different seceral agamic complexes. Therefore, apomixis is not a major factor in evolution; however, it is important in increasing the polymorphism and the geographic distribution of the cultivars where it is found. For the apomictic plant breeding in commercial terms, many universities, national and international institutes, state and private research centers and multinational seed organisations are investing on this topic such as University of Harvard, University of Georgia, CSIRO, CIMMYT, USDA-ARS, IRD, CNR, NIVOT, CPRODLO, CIAT, IRRI, NIOO-KNAW, Advanta, Dupond, Limagrain Group, Novartis, Sudwestdeutsche Saatzucht, Deutsche Saatveredelung Lippstad, etc. In all over the world (Asker and Jerling, 1992; Dresselhaus and Colombo, 2001; Kaushal et al., 2004). All multidisciplinary approach of using both sexual model species and apomictic breeding techniques will be make easy the isolation of key the genetic factors controlling apomixis in the near future, but, still low seed setting, low male fertility or low fertility level are the most important constraints (Ulukan, 2009a). And if these hindrances could be overed in terms of biologically and agronomically with the multidisciplinear approach, new horizons will be open for the world beyond the humanity (Ulukan, 2009b).
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