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Ecological Anatomy in Halophytes with C4 Photosynthesis: Discussing Adaptative Features in Endangered Ecosystems

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Ecological Anatomy in Halophytes with C4 Photosynthesis: Discussing Adaptative Features in Endangered Ecosystems Carpathian Journal of Earth and Environmental Sciences, May 2012, Vol. 7, No. 2, p. 13 - 21 ECOLOGICAL ANATOMY IN HALOPHYTES WITH C4 PHOTOSYNTHESIS: DISCUSSING ADAPTATIVE FEATURES IN ENDANGERED ECOSYSTEMS Marius-Nicuşor GRIGORE1, Constantin TOMA1, Maria-Magdalena ZAMFIRACHE1, Monica BOSCAIU2, Zenovia OLTEANU1 & Dumitru COJOCARU1 1 Alexandru Ioan Cuza University, Faculty of Biology, Bd. Carol I, 20 A, 700505, Iasi, Romania, e-mail: [email protected]; 2 Instituto Agroforestal Mediterráneo (UPV), CPI, edificio 8E, Universidad Politécnica de Valencia, Camino de Vera s/n, 46022 Valencia, Spain, e-mail: [email protected]; Abstract. The Chenopodiaceae halophyte species provide perhaps the ideal model to study the ecological adaptations in relations with extreme environmental conditions. Closely linked with saline habitats, the chenopods with Kranz anatomy represents a striking and intriguing example of coevolution. In this study, we investigate the Kranz anatomy in a holistic manner in halophytes vegetating in two nature reserves, here regarded as rare and endangered ecosystems. This issue, apart from its scientific interest – as an adaptive, ecological and evolutive feature – also suggests the compulsory necessity to protect these areas, in order to preserve the floristic diversity in such menaced ecosystems. Keywords: halophytes, Kranz Anatomy, C4 photosynthesis, strategy, evolution, adaptation. 1. INTRODUCTION reproduce in saline environments; despite the progresses recorded in the last decades, it is still The Earth’s surface area occupies about 13.2 very difficult to use a single-conventional definition billion ha, but no more than 7 billion ha are arable of halophytes (Grigore, 2008a; 2008b; Grigore & and 1.5 billion are cultivated (Massoud, 1981). Of Toma, 2010a; Grigore & Toma, 2010b). the cultivated lands, about 340 million ha (23%) are C4 photosynthesis is a series of biochemical saline (salt-affected) and another 560 million ha and anatomical modifications that concentrate CO2 (37%) are sodic (sodium-affected) (Tanji, 2002). around the carboxylating enzyme Rubisco (Sage, Here are many different projections, suggesting that 2004). This photosynthetic type is not a single human population will increase over 8 billion by the metabolic pathway; it is a series of biochemical and year 2020 that will worsen the current scenario structural adjustments that have exploited about food insecurity (Athar & Ashraf, 2009). There phosphoenolpyruvate carboxylase (PEPCase) and are often not sufficient reservoirs of freshwater other existing enzymes to concentrate CO2 around available and most of the agronomically used Rubisco. irrigation systems are leading to a permanent In the great majority of C4 plants, increase in the soil-salinity and slowly to growth functioning of the C4 pathway requires metabolic conditions inacceptable for most of the common cooperation of two closed and distinct crops (Koyro et al., 2009). chlorenchymatous tissues: an external one (or Salt stress, together with water stress, became, photosynthetic carbon assimilative - PCA) and an in above described circumstances, one of the most inner bundle sheath (or photosynthetic carbon interesting studied issue over the last years reductive - PCR) tissues. These tissues are arranged (Cheeseman, 1988; Shannon, 1992; Bohnert et al., concentrically with respect to vascular tissues, 1995; Neumann, 1997; O’Leary, 2002; Sen et al. forming a structural pattern known as Kranz 2002; Yokoy et al., 2002). anatomy (Muhaidat et al., 2007). This structural type Halophytes are plants able to vegetate and provides one of the best examples of the intimate 13 connection between plant form and function and halophyte (Şerbănescu, 1965). Remaining species represents a suite of structural characters that have have been considered as obligatory halophytes evolved repeatedly from C3 ancestors (Dengler & (Ţopa, 1954; Şerbănescu, 1965), euhalophytes Nelson, 1999; Kellog, 1999; Sage, 2001; Sage, (Bucur, 1960). Anyway, attention should be paid on 2004). This internal architecture physically the fact that in Aronson’s database (1989) refering partitions the biochemical events of the C4 pathway on halophytes, only P. crassifolia and A. tatarica into two main phases. In the first step, atmospheric have been included in. This could be explained by CO2 is initially assimilated into C4 acids by PCA- limited inputs in collating this database. In addition, tissue-specific phosphoenolpyruvate carboxylase. In appart from A. tatarica, considered as weedy plant the second phase, these acids diffuse into the PCR and having a wide distribution in Europe, other taxa compartment, where they are decarboxylated, and have a quite restricted distribution in Europe. the released CO2 is re-fixed by PCR-tissue-specific Camphorosma monspeliaca occurs in saline soils Rubisco. This biphasic C4 system enhances CO2 and dry waste places, and it is confined to South of levels around Rubisco, suppressing photorespiration Europe, extending northwards to 530 North In East and improving plant carbon balance (Kanai & Russia while C. annua vegetates in saline habitats, Edwards, 1999). restricted to East and Center of Europe, extending to The aim of our work is to integrate the Kranz Bulgaria and Central Ukraine (Edmonson, 1993). anatomy structure in the whole set of adaptive Petrosimonia species, all growing in saline habitats, features of halophytes, especially addressing to have a more local distribution, occuring only in ecological factors. Our investigations refer to five South East of Europe (Albania, Romania and halophyte species; four of these have a limited Russia) (Edmonson, 1993); in Romania, P. distribution in Europe, as described above. In oppositifolia is a very rare species (Grigore, 2008a). addition, several of investigated species were ‚Valea Ilenei’ (Iaşi) is a quite small but very collected from two nature reserves. Therefore, interesting natural reserve of saline soils from discussing this evolutive pattern also referring to Romania. It occupies only 10 hectares and is located such fragile ecosystems could reveal several new to approximately 4 km NV from Letcani rail station, aspects related to interrelations plant-soil. at confluence of Valea Ilenei and Bahlui rivers (Nicoară & Bomher, 2010). Data regarding the flora 2. MATERIAL AND METHODS and vegetation of this unique nature reserve are very scattered (Burduja, 1939; Răvărut, 1941; Mititelu, 2.1. Material eta al., 1987). Recently, a preliminary study regarding the ecology of halophytes in this area has The material subjected to our analysis is been published (Grigore & Toma, 2011), but the represented by leaves of halophytes, collected from “Valea Ilenei’ nature reserve still requires a special saline habitats, in plants anthesis phenophase. The attention and long-term monitoring studies. As we taxa subjected to our investigations are: Atriplex revealed (Grigore & Toma, 2011) this limited- tatarica L., Camphorosma annua Pall., surface reserve provides perhaps the most striking Camphorosma monspeliaca L., Petrosimonia habitat where interrelationships halophytes- oppositifolia (Pall.) Litv. and Petrosimonia triandra ecological factors are to be deeply studied. The large (Pall.) Simonk, from Chenopodiaceae family. P. biodiversity, referring on microhabitats, as well on oppositifolia has been collected from a salty habitat, specific flora in this reserve argue again for on Cotnari (Iaşi) from a salinized slope on Belceşti extending the researches in this reserve. (Iaşi), C. annua and A. tatarica from ‘Valea Ilenei’ ‘Fâneţele seculare de la Valea lui David’ (Iaşi) (Iaşi) natural reserve, P. triandra and C. is a floristic reserve, located to approximately 5 km V monspeliaca from ‘Valea lui David’ (Iaşi), during from Iaşi, at 1000 m from Iaşi-Targu Frumos road years of 2005-2007. (Nicoară & Bomher, 2010). As in the case of ‘Valea The ecological characterization, our short Ilenei’, here also vegetate many rare, vulnerable and notes in the field as well as other histo-anatomical endemic species, also included in ‘Cartea Roşie a features suggest that all investigated taxa are xero- judeţului Iaşi’ (Nicoară & Bomher, 2010). halophytes (Grigore and Toma, 2010a), appart from A. tatarica, which is a species with a wider 2.2. Methods ecological spectrum, a non-obligatory halophyte. This species has been classified by Romanian plant For subsequent histo-anatomical ecologists as preferential halophyte (Ţopa, 1954), investigations, the material was fixed and preserved neohalophyte (Bucur, 1961) and supporting in ethanol (70°). 14 Leaf cross sections were obtained using a photosynthesis and implicitly Kranz anatomy (Sage razor blade and a microtome. The cross sections et al., 1999a). obtained were subsequently subjected to the In Petrosimonia oppositifolia, we evidenced in “classical” stages of a common histo-anatomical the structure of lamina, the kochioid Kranz anatomy procedure: immersion in sodium hypochlorite for sub-type (Fig. 3), also related with C4 photosynthesis. 20-30 min, washing with acetic water and tap water, The cross sections must be analyzed carefully, then staining: first with iodine green (for 1 minute) because the continuous/discontinuous character of and washing in ethanol (90°) bath then second with internal chlorenchyma imposes the true “diagnosis” red carmine (for 20 min.), washing with water and regarding different sub-types. The kochioid finally fixation in glycerol-gelatine. configuration is very similar to the salsoloid one, the Permanent
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