Impatiens is one of the two genera of the family Balsaminaceae (order: Geraniales) that has about 1000 species (Caris et al., 2006). Around 850 species of Impatiens are annual and perennial herbs and shrubs (Llamas, 2003). The Himalayan region is proposed as Impatiens's origin and the major centers of diversity are in the highlands and mountains of sub-tropical and tropical of Africa and South Asia (Uchneat, 2007). Impatiens native species are absent from Australia and South America (Caris et al., 2006).
Plants of Impatiens have a relatively long flowering season, generally ranging through summer and fall (Cosner, 2003). The commercially significant species of Impatiens are I. hawkeri, I. walleriana, and I. balsamina. I. hawkeri plants do not cross with the I. walleriana species, nor is it believed to cross with I. balsamina. Although I. walleriana plants generally are more vigorous than I. hawkeri, I. walleriana flowers are less bright and smaller than I. hawkeri ones. In addition, Impatiens hawkeri plants are larger and their petals are more durable (Cosner, 2003).
New Guinea impatiens
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New Guinea impatiens hybrids have been developed by crossing different species of Impatiens with I. hawkeri. They are native from New Guinea and the surrounding islands, where they have been grown for generations by the Papuans (Indigenous from New Guinea). They collected and traded with the plants actively, selected the showier varieties and planted them around their villages for ornament. Although NGI has been in general cultured since 1886, it was not before 1970 that the species was crossed with others varieties from the region to produce attractive hybrids plants (Morgan, 2007).
In recent years, the development of the global horticultural industry has gained many millions of dollars annually, and the most important focus has been on the sale of annual breeding and patio plants (Morgan, 2007). Annual breeding plants are the largest (45%) section of the United States (U.S.) in the commercial floriculture trades, with a reported wholesale value in 2007 of $1.76 billion (U.S. Department of Agriculture, 2008). In 2006, US imported 878 million non-rooted cuttings with a reported wholesale value of US $61 million (U.S. Department of Agriculture, 2007) (Lopez and Runkle, 2008 b). Sales of Impatiens genus varieties are estimated at 250 million dollars per year. A huge part of this business is attributable to the sale of I. walleriana and I. hawkeri hybrids (Morgan, 2007). New Guinea plants are economically important, and very popular in the floriculture trade (Morgan, 2007).The global demand of NGI cuttings has achieved a volume up to 100 million plants annually (Lopez and Runkle, 2008 a).
NGI plants are in the top 10 of the German bed and balcony plants. According to Federal statistical, in Germany (2000), around 13.8 million units of NGI, were produced. In 2004 the major growing regions of NGI were North Rhine-Westphalia, Bavaria, Baden-Wuerttemberg and Lower Saxony (Hanke, 2008).
Arbuscular mycorrhiza (AM) (meaning fungus from the Greek 'mycos' and meaning root from 'rhiza') is a symbiotic association between soil fungi and plant root. It has been found that between 90% and 95% of plants have mycorrhizal fungi associated with them (Entry et al., 2002), being AM the most common mycorrhiza association. The mycorrhization, is a process where both organisms obtained benefits. The fungi acquires carbon from their host plants to complete their life cycle, in return, these microorganisms provide many benefits for the plant, including improved mineral nutrition and enhanced tolerance to different types of stresses (Smith and Read 2008; Xian-Can et al., 2009).
Because arbuscular mycorrhiza fungi (AMF) are obligate biotroph, there are many difficulties culturing AMF without a plant host. Therefore the classification of AM was based almost completely on the wall structure and development of the fungi's spores.
Until recent studies, AMF were most closely related to the phylum Zygomycota and not to the phylum Glomeromycota, because their non septate hyphae and despite of absence of typical sexual stages. The use of molecular techniques (DNA sequences) allowed doing a new evaluation for provide a comprehensive idea of AMF classification (Smith and Read, 2008) that includes one class, four orders, nine families and ten genera:
Morphology and Biology
It has been possible to define two simple morpholigical types of AM fungi, the Arum-type and the Paris-type, these types were designated after they were found in plants of Arum maculatum and Paris quadrifoli, respectively. In the Arum-type, fungi form intercellular hyphae between the cortical cells and intracellular arbuscules within them. The Paris-type is characterized by extensive intracellular hyphal and arbusculate coils in the root cortex (Cavagnaro et al., 2001). Smith and Smith (1997) reported that 41 families are part of the Paris-type, 30 families of the Arum-type and 21 families are an intermediate morphology or have members with both Paris and Arum-type.
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The fungus hyphal growth starts with the spore germination, subsequently the root surface and cortex of the plant are penetrated by the appressorium. Then the hypha penetrates the cell walls and develops tree-like structures, called arbuscules, within the cortex cells, by repeated dichotomous branching. An important feature of AMF is the arbuscule, responsible for nutrient exchange. Each fungal branch within a plant cell is surrounded by a plant-derived periarbuscular membrane (PAM). The apoplastic interface between the fungal plasma membrane and the plant-derived PAM is called the periarbuscular space (PAS) (Parniske, 2008).
During the germination of the spores and the hyphae growth the stimulatory effect of plant root exudates plays a key role. The strogolactones are a kind of phytohormones that when are recognized by the fungus induces a pre-symbiotic stage. This stage is characterized by the spore germination, followed by the hyphal growth, and hyphae branching. Then fungi produce mycorrhiza factors that induce changes in the calcium concentration in the epidermal root cells and activate plant symbiosis-related genes. AMF has special types of appressorium (developed from mature hyphae) to reaches the plant roots. Plant cells produce a pre-penetration apparatus (PPA) and subsequently fungal hyphae enter the PPA, which guides the fungus until reaches the cortex (Parniske, 2008).
Host range and specificity
The AM fungi have extremely wide range of potential plants for mycorrhizal associations. It develops in most angiosperm and gymnosperms, also ferns and lycopods. Within the angiosperm group the dicotyledonae has been observed to have more incidences in mycorrhizas symbioses than monocotyledonae class (Smith and Read, 2008).
It is considered that arbuscular mycorrhizal has not absolute specificity, because a given AM species can colonize a range of plant species and a given plant species can be colonized by several different AM species. There are about 150 species of arbuscular mycorrhizal fungi which have mutualistic symbiotic associations with the roots of about 80-90 % (approximately 200,000 plants) of terrestrial plant species. This indicates a low fungus to host species ratio, and because of this, it is believed that the AMF are not host-specific. It means that each fungal species theoretically must have many hosts. Practical observation in the field indicates that single plant root systems can contain many AM fungi and that different plant species at the same site often contain the same fungi (Smith and Read, 2008).
It is well established that AM roots are often more efficient in nutrient acquisition, per unit length than non-colonized roots (Merryweather and Fitter, 1998). Phosphorous (P) is believed to be the major nutrient that is being absorbed by AM. Since P is poorly mobile in soil and occurs in very low concentrations in the soil solution, being rapidly fixed as iron, aluminum or calcium phosphate or immobilized in the microbial biomass, it is poorly absorbed by plants. It has also been found that AM increased the uptake of zinc, which is also poorly mobile and is deficient in some soils, and copper. Recently, the attention has turned to nitrogen which, in addition to its organic forms, occurs as either poorly mobile ammonium or nitrate; the latter is highly mobile in moist soil, but not in dry soil. It is becoming clear that AM fungi have the potential to play a considerable part in plant N nutrition and that uptake of both ammonium and nitrate can be increased in mycorrhizal plants. Some mechanisms of AM for increasing the nutrients uptake are the exploration of a larger soil volume and increase the area of up taking surface (Smith and Read, 2008).
The effect of arbuscular mycorrhizal fungi on pathogens and insect herbivores are in most of the cases indirect, and result from altered physiology plant and increase nutrition of the host. AM fungi may increase the host tolerance by improving root growth and function. AMF also may enhance host resistance (decrease pathogen performance) by altering root exudations used by pathogens or stimulating a defense reply (Borowicz, 2001). Some studies have reported that AMF compete directly with other biotrophic organisms for photosynthate for the same cortical space and resources, suppressing the growth of pathogen (Smith and Read, 2008).
Gaur et al. (2000) reported that mycorrhization improved nutrient uptake (P and K), vegetative growth (shoot height and dry matter) (Table 1) and flower production in the ornamental plants: Petunia hybrida, Callistephus chinensis and Impatiens balsamina. Xian-Can et al. (2009) found that at optimal and low temperature, arbuscular mycorrhiza colonization enhances the concentrations of chlorophyll (Chl) a, Chl b and Chl a+b. Non mycorrhitical plants decreased the synthesis rate of chlorophyll and enhanced the Chl and chloroplast damage reducing the photosynthetic rate.
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Table 1. Influence of inoculation with mixed AM on growth and nutrient uptake of Petunia hybrid, Callistephus chinensis and Impatiens balsamina (Gaur et al., 2000)
It is widely recognized the importance of plant nutrition (mineral elements) for plant growth and development. Plants without essential minerals are not able to complete their life cycle. Mineral elements are constituents of enzyme molecules and organic compounds (proteins, nucleic acids), besides they are directly or indirectly involved in plant metabolism. It is often recognized that the growth of the plants is related with a high photosynthetic activity; and the photosynthesis process directly related with different mineral nutrients, such as Mg. Mn, Fe, S and Cu. In PS II and PS I chlorophyll molecules with the central magnesium atom absorb photons, initiating the electron flow of the electron transport chain, also the splitting of the water in the PSII is related with the manganese mineral-containing enzyme complex (Marschner, 1985)
Plants with an optimum nutritional status often are healthy; therefore it is expected to be more resistant to environmental stresses than plants with a not adequate nutritional level. Cropaid (biofertlizer/plant strengthener) contains a mixture of minerals and the Thiobacillus spp. bacteria, that improving plant nutrition and make them tolerant to cold stress conditions.
Cropaid biomineral content is easily absorbed by the leaves, stem and roots of the plants; in a short period of time the plants begin to have heavy metabolic activity and their content of amino-acids, proteins, and sugar will increase. Because of Cropaid improve the photosynthesis capability and other metabolic activities, it make the plants stronger against the enviromental stress conditions, including low temperature (Cropaid xx).
Plants have evolved to exist in conditions which sometimes are not ideal for maintenance of normal physiology and may be imitated the survival (Shepherd and Griffiths, 2006). The stress includes any environmental factor with the capacity to induce a physical or chemical change, independently whether the change is beneficial or detrimental to the organism (Entry et al., 2002). The abiotic stress for the plant arises from exposure to extremes climatic conditions such as frost, cold, heat, altitude, radiation levels, shade, water status and pollution (Shepherd and Griffiths, 2006). In response, the plants can show avoidance or tolerance as two types of adaptive behavior (Osmond et al., 1987).
The stress due to low or high temperatures can affect the photoperiodic response of the plants. Some ornamental species are sensitive to high night temperatures such as Tagetes erecta, Euphorbia pulcherrima, and Gomphrena globosa, other species are sensitive to high day temperatures (Antirrhinum majus), and some species like NGI are sensitive to high day or night temperatures (Uchneat, 2007).
Low temperature is one of the most important abiotic stresses that affect the growth and natural distribution of plants species (Xian-Can et al., 2009). When chilling-sensitive plants are exposed to low temperature between 0°C and 12°C (Allen and Ort, 2001) they may suffer physiological and metabolic changes.
The response of plants to low temperatures is usually dependent of the climatic conditions of the areas from where the crops ´origins. Plants originating in temperate regions are usually much more tolerant to low temperatures than plants from subtropical and tropical regions, and their metabolism and growth are quickly reversed when the temperature rise. Tropical and subtropical plants that grow in temperate regions are sensible to low temperatures since they have not developed successful acclimatory responses like native plants (Baker and Rosenqvist, 2004).
New Guinea impatiens plants have relative warm optimal temperature between 18°C and 21°C. The temperature at which the development of New Guinea impatiens stops, is between 10 °C to 13°C (Lopez and Runkle, 2008 a).
Physiological response to chilling stress
Low temperature decreases the growing of the plant and reduces the efficiency of photosynthesis due to changes in pigment composition and damages in the chloroplastic development (Farooq et al., 2009). Cool temperatures, also includes changes in carbohydrate metabolism, respiration rates and cellular lipid composition (Wang et al., 1997). All these plant responses to chilling stress appear to be related with injury in the membranes, followed by loss of the function. Damage in membranes of chloroplasts and mitochondria affect the plant photosynthesis and respiration. Tropical and subtropical plants that are chilling sensible, have many saturated fatty acid chains in the lipids of the cell membrane, therefore to low temperatures the membranes tend to be less fluid and become to semisolid stage. The damage in the membranes means loss of the activity in the transport of ions, solutes, and proteins into and out the cell. On the other hand, chilling tolerant plants have a high proportion of unsaturated lipids that permit to the membranes to be more fluid at low temperatures than chilling sensible plants. During acclimation to low temperatures, tolerant plants increase the activity of desaturase enzymes and the amount of unsaturated fatty acid chains. Plants exposed to freezing temperatures (under 0ËšC), form small ice crystals in intercellular spaces and in the xylem vessels due to the temperature is below of the freezing point of water. Some crystals could damage the cell causing cellular death. Plants exposed to freezing temperatures for long time suffer dehydration due to the movement of liquid water from inside the cell to the extracellular ice crystal xxxx.
Chlorophyll a Fluorescence
Photosynthesis process is initiated when light energy is absorbed by the antenna molecules within the photosynthetic membrane (Strasser et al., 2000). Light energy absorbed by chlorophylls (Chls) associated with photosystem II (PSII) can be used to drive photochemistry, in which an electron is transferred from the reaction center Chl, P680, to the primary quinone acceptor (QA) of PSII. Otherwise, absorbed light energy can be lost from PSII as heat or Chl a fluorescence. The processes of photochemistry, Chl a fluorescence, and heat loss are in direct competition for excitation energy. If the rate of one process (photochemistry, Chl a fluorescence or heat lost) increases the rates of the other two will decrease (Figure 1) (Baker, 2008).
Figure 1. Simple model of the possible fate of light energy absorbed by PSII (Baker, 2008).
The photosynthetic apparatus responds to the particular changes in energy balance caused by biotic and abiotic stresses (Krause, 1991). The chlorophyll a fluorescence (emitted by green plants) is a very small fraction of the dissipated energy from the photosynthetic apparatus that has made the fluorescence technique an important tool in the applied and basic plant physiology research The Chl a fluorescence is a fast, non-destructive and relatively simple method used widely to investigate the response of plants to the metabolic and energetic imbalance of photosynthesis caused by stress (Araus et al., 1998), including the effects of low temperature.
JIP test and Performance Index (PI)
When a leaf is adapted to dark and then exposed to light energy, changes in Chl fluorescence occur. The sequence of phases from initial (Fo) (PSII reaction centers are in the 'open' state) to the maximal (Fm) fluorescence value have been labeled O, J, I, P fluorescence transient, and its shape changes under different environmental stress, such as temperature, light or drought (Tsimilli-Michael et al., 2000). Numerous studies have only used the ratio of the variable to the maximal Chl a fluorescence (Fv/ Fm, Fv= Fm-Fo) as parameter to screen for chilling tolerance. However, in some cases insensitivity to chilling has been shown (Strauss et al., 2006). Strasser et al. (2000) introduced a multi-parametric expression, called performance index (PI), which Strauss et al. (2006) suggests like an appropriate parameter for evaluating a large number of genotypes for dark chilling tolerance. The PI index takes into consideration the major functional steps of photosynthetic activity by a PSII reaction center complex: 1.light energy absorption, 2.trapping of excitation energy, and 3.conversion of excitation energy to electron transport (Strauss et al., 2006).
Pinior et al. (2005) reported that analysis of Chl a fluorescence using the JIP test prove to be an indicator marker for AM-induced drought tolerance in rose plants, indicating that arbuscular mycorrhiza fungi increase the electron flow and the productive photosynthetic activity at many sites of the photosynthetic electron transport chain. The derived PI index illustrates the enhanced vitality of AM plants under drought and the reduction of the photosynthetic activity of non AM plants (Figure 2). Strasser et al. (2007) reported that the performance index (biophysical parameter) is correlated with physiological measures (plant height) in chick peas plants inoculated with AMF (G. mosseae and G. caledonium) and Piriformospora indica under cadmium stress.
Figure 2. Performance index [PI (abs)] of rose plants inoculated with G. intraradices (+myc) and without mycorrhiza (−myc) before stress (− stress), during severe stress (+ stress), and during recovery (r1, r2, r3) (Pinior et al., 2005).