Abstract
C4 species of family Chenopodiaceae, subfamily Suaedoideae have two types of Kranz anatomy in genus Suaeda, sections Salsina and Schoberia, both of which have an outer (palisade mesophyll) and an inner (Kranz) layer of chlorenchyma cells in usually semi-terete leaves. Features of Salsina (S. aegyptiaca, S. arcuata, S. taxifolia) and Schoberia type (S. acuminata, S. eltonica, S. cochlearifolia) were compared to C3 type S. heterophylla. In Salsina type, two layers of chlorenchyma at the leaf periphery surround water-storage tissue in which the vascular bundles are embedded. In leaves of the Schoberia type, enlarged water-storage hypodermal cells surround two layers of chlorenchyma tissue, with the latter surrounding the vascular bundles. The chloroplasts in Kranz cells are located in the centripetal position in Salsina type and in the centrifugal position in the Schoberia type. Western blots on C4 acid decarboxylases show that both Kranz forms are NAD-malic enzyme (NAD‐ME) type C4 species. Transmission electron microscopy shows that mesophyll cells have chloroplasts with reduced grana, while Kranz cells have chloroplasts with well-developed grana and large, specialized mitochondria, characteristic of NAD‐ME type C4 chenopods. In both C4 types, phosphoenolpyruvate carboxylase is localized in the palisade mesophyll, and Rubisco and mitochondrial NAD‐ME are localized in Kranz cells, where starch is mainly stored. The C3 species S. heterophylla has Brezia type isolateral leaf structure, with several layers of Rubisco-containing chlorenchyma. Photosynthetic response curves to varying CO2 and light in the Schoberia type and Salsina type species were similar, and typical of C4 plants. The results indicate that two structural forms of Kranz anatomy evolved in parallel in species of subfamily Suaedoideae having NAD‐ME type C4 photosynthesis.
Key words
C3 plants - C4 plants - Chenopodiaceae - chloroplast ultrastructure - immunolocalization - NAD‐ME type - photosynthetic enzymes -
Suaeda spp
References
1
Aliscioni S. S., Giussani L. M., Zuloaga F. O., Kellogg E. A..
A molecular phylogeny of Panicum (Poaceae: Paniceae): Tests of monophyly and phylogenetic placement within the Panicoideae.
American Journal of Botany.
(2003);
90
796-821
2
Behnke H.-D..
Sieve-element characters.
Nordic Journal of Botany.
(1981);
1
381-400
3
Bil K. J., Ljubimov V. Y., Trusov M. F., Gedemov T., Atachanov B. O..
The participation of three types of autotrophic tissue in diurnal dynamic of CO2 assimilation in some Chenopodiaceae species.
Botanicheskii Zhurnal.
(1983);
68
54-61
4
Bil K. Y., Lyubimov V. Y., Demidova R. N., Gedemov T..
Assimilation of CO2 by plants of Chenopodiaceae family with three types of autotrophic tissues in the leaves.
Soviet Plant Physiology.
(1982);
28
808-815
5
Bil K. J., Gedemov T..
Features of the structure and function of assimilation apparatus of Suaeda arcuata Bunge (fam. Chenopodiaceae) connected with cooperative photosynthesis.
Doklady Akademii Nauk SSSR, Comptes rendus de l'Académie des Sciences de l'URSS.
(1980);
250
1014-1017
6
Brooks A., Farquhar G. D..
Effect of temperature on the CO2 /O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light.
Planta.
(1985);
165
397-406
7
Brown W. V..
Variations in anatomy, associations, and origin of Kranz tissue.
American Journal of Botany.
(1975);
62
395-402
8
Brown W. V..
The Kranz syndrome and its subtypes in grass systematics.
Memoires of the Torrey Botanical Club.
(1977);
23
1-97
9
Carolin R. C., Jacobs S. W. L., Vesk M..
The structure of the cells of the mesophyll and parenchymatous bundle sheath of the Gramineae.
Botanical Journal of the Linnean Society.
(1973);
66
259-275
10
Carolin R. C., Jacobs S. W. L., Vesk M..
Leaf structure in Chenopodiaceae.
Botanische Jahrbücher für Systematische Pflanzengeschichte und Pflanzengeographie.
(1975);
95
226-255
11
Carolin R. C., Jacobs S. W. L., Vesk M..
Kranz cells and mesophyll in the Chenopodiales.
Australian Journal of Botany.
(1978);
26
683-698
12
Carolin R. C., Jacobs S. W. L., Vesk M..
The chlorenchyma of some members of the Salicornieae (Chenopodiaceae).
Australian Journal of Botany.
(1982);
30
387-392
13 Dengler N. G., Nelson T.. Leaf structure and development in C4 plants. Sage, R. F. and Monson, R. K., eds. C4 Plant Biology. Physiological Ecology Series. San Diego; Academic Press (1999): 133-172
14
Edwards G. E., Franceschi V. R., Voznesenskaya E. V..
Single cell C4 photosynthesis versus the dual-cell (Kranz) paradigm.
Annual Review of Plant Biology.
(2004);
55
173-196
15
Fisher D. D., Schenk H. J., Thorsch J. A., Ferren Jr. W. R..
Leaf anatomy and subgeneric affiliation of C3 and C4 species of Suaeda (Chenopodiaceae) in North America.
American Journal of Botany.
(1997);
84
1198-1210
16
Freitag H., Stichler W..
A remarkable new leaf type with unusual photosynthetic tissue in a central Asiatic genus of Chenopodiaceae.
Plant Biology.
(2000);
2
154-160
17
Freitag H., Stichler W..
Bienertia cycloptera Bunge ex Boiss., Chenopodiaceae, another C4 plant without Kranz tissues.
Plant Biology.
(2002);
4
121-132
18
Gamaley Y. V..
The variations of the Kranz-anatomy in Gobi and Karakum plants.
Botanicheskii Zhurnal.
(1985);
70
1302-1314
19
Gamaley Y. V., Glagoleva T. A., Koltschevsky K. G., Chulanovskaya M. V..
The C4 -syndrome type ecology and evolution in connection with phylogeny of the Chenopodiaceae and Poaceae.
Botanicheskii Zhurnal.
(1992);
77
1-12
20
Giussani L. M., Cota-Sanches J. H., Zuloaga F. O., Kellogg E. A..
A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis.
American Journal of Botany.
(2001);
88
1993-2012
21
Glagoleva T. A., Chulanovskaya M. V., Pakhomova M. V., Voznesenskaya E. V., Gamaleï Y. V..
Effect of salinity on the structure of assimilating organs and 14 C labelling patterns in C3 and C4 plants of Ararat plain.
Photosynthetica.
(1992);
26
363-369
22
Glagoleva T. A., Voznesenskaya E. V., Kolchevsky K. G., Kocharyan N. I., Pakhomova M. V., Chulanovskaya M. V., Gamaley Y. V..
Structural and functional characteristics of halophytes from the Ararat.
Fiziologiya Rastenii.
(1990);
37
1080-1088
23
Glagoleva T. A., Zeynalova M. G., Gamaley Y. V..
Structural and functional characteristics of succulent desert plants of the Chenopodiaceae family.
Botanicheskii Zhurnal.
(1987);
72
1175-1186
24
GPWG .
Phylogeny and subfamilial classification of the grasses (Poaceae).
Annals of the Missouri Botanical Garden.
(2001);
88
373-457
25
Guralnick L. J., Edwards G. E., Ku M. S. B., Hockema B., Franceschi V. R..
Photosynthetic and anatomical characteristics in the C4 -Crassulacean acid metabolism-cycling plant, Portulaca grandiflora .
Functional Plant Biology.
(2002);
29
763-773
26
Gutierrez M., Gracen V. E., Edwards G. E..
Biochemical and cytological relationships in C4 plants.
Planta.
(1974);
119
279-300
27
Hatch M. D., Kagawa T., Craig S..
Subdivision of C4 -pathway species based on differing C4 acid decarboxylating systems and ultrastructural features.
Australian Journal of Plant Physiology.
(1975);
2
111-128
28 Hattersley P. W.. Variations in photosynthetic pathway. Soderstrom, T. R., Hilu, K. W., Campbell, C. S., and Barkworth, M. E., eds. Grass Systematics and Evolution. London; Smithsonian Institution Press Washington, D.C. (1987): 49-64
29
Hattersley P. W., Browning A. J..
Occurrence of the suberized lamella in leaves of grasses of different photosynthetic types. I. In parenchymatous bundle sheaths and PCR (“Kranz”) sheaths.
Protoplasma.
(1981);
109
371-401
30
Jacobs S. W. L..
Review of leaf anatomy and ultrastructure in the Chenopodiaceae (Caryophyllales).
The Journal of the Torrey Botanical Society.
(2001);
128
236-253
31
Kadereit G., Borsch T., Weising K., Freitag H..
Phylogeny of Amaranthaceae and Chenopodiaceae and the evolution of C4 photosynthesis.
International Journal of Plant Sciences.
(2003);
164
959-986
32
Kapralov M. V., Akhani H., Voznesenskaya E., Edwards G., Franceschi V. R., Roalson E. H..
Phylogenetic relationships in the Salicornioideae/Suaedoideae/Salsoloideae s.l. (Chenopodiaceae) clade and a clarification of the phylogenetic position of Bienertia and Alexandra using multiple DNA sequence datasets.
Systematic Botany.
(2006);
31
571-585
33
Kiirats O., Lea P. J., Franceschi V. R., Edwards G. E..
Bundle sheath diffusive resistance to CO2 and effectiveness of C4 photosynthesis and refixation of photorespired CO2 in a C4 cycle mutant and wild-type Amaranthus edulis.
.
Plant Physiology.
(2002);
130
964-976
34
Koch K., Kennedy R. A..
Characteristics of Crassulacean Acid Metabolism in the succulent C4 dicot, Portulaca oleracea L.
Plant Physiology.
(1980);
65
193-197
35
Ku M. S. B., Edwards G., Tanner C. B..
Effects of light, carbon dioxide, and temperature on photosynthesis, oxygen inhibition of photosynthesis, and transpiration in Solanum tuberosum.
.
Plant Physiology.
(1977);
59
868-872
36
Lara M. V., Drincovich M. F., Andreo C. S..
Induction of a crassulacean acid-like metabolism in the C4 succulent plant, Portulaca oleracea L.: Study of enzymes involved in carbon fixation and carbohydrate metabolism.
Plant and Cell Physiology.
(2004);
45
618-626
37
Liu Y., Dengler N. G..
Bundle sheath and mesophyll cell differentiation in the C4 dicotyledon Atriplex rosea : quantitative ultrastructure.
Canadian Journal of Botany.
(1994);
72
644-657
38
Long J. J., Berry J. O..
Tissue-specific and light-mediated expression of the C4 photosynthetic NAD-dependent malic enzyme of amaranth mitochondria.
Plant Physiology.
(1996);
112
473-482
39
Maurino V. G., Drincovich M. F., Andreo C. S..
NADP-malic enzyme isoforms in maize leaves.
Biochemistry and Molecular Biology International.
(1996);
38
239-250
40
O'Brian T. P., Carr D. J..
A suberized layer in the cell walls of the bundle sheath of grasses.
Australian Journal of Biological Sciences.
(1970);
23
275-287
41
Ohsugi R., Murata T., Chonan N..
C4 syndrome of the species in the Dichotomiflora group of the genus Panicum (Gramineae).
Botanical Magazine Tokyo.
(1982);
95
339-347
42
Pyankov V. I., Kuz'min A. N., Demidov E. D., Maslov A. I..
Diversity of biochemical pathways of CO2 fixation in plants of the families Poaceae and Chenopodiaceae from the arid zone of Central Asia.
Soviet Plant Physiology.
(1992);
39
411-420
43
Pyankov V. I., Vakhrusheva D. V..
Pathways of primary CO2 fixation in C4 plants of the family Chenopodiaceae from the arid zone of Central Asia.
Soviet Plant Physiology.
(1989);
36
178-187
44
Pyankov V. I., Voznesenskaya E. V., Kuz'min A. N., Ku M. S. B., Ganko E., Franceschi V. R., Black Jr. C. C., Edwards G. E..
Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae).
Photosynthesis Research.
(2000);
63
69-84
45 Sage R. F., Li M., Monson R. K.. The taxonomic distribution of C4 photosynthesis. Sage, R. F. and Monson, R. K., eds. C4 Plant Biology. New York; Academic Press (1999): 551-584
46
Schütze P., Freitag H., Weising K..
An integrated molecular and morphological study of the subfamily Suaedoideae Ulbr. (Chenopodiaceae).
Plant Systematics and Evolution.
(2003);
239
257-286
47
Shojima S., Nishizawa N. K., Mori S..
Do intrathylakoidal inclusions really contain RuBPCase?.
Protoplasma.
(1987);
140
187-189
59
Shomer-Ilan A., Beer S., Waisel Y..
Suaeda monoica , a C4 plant without typical bundle sheaths.
Plant Physiology.
(1975);
56
676-679
48
Shomer-Ilan A., Neumann-Ganmore R., Waisel Y..
Biochemical specialization of photosynthetic cell layers and carbon flow paths in Suaeda monoica .
Plant Physiology.
(1979);
64
963-965
49
Shomer-Ilan A. S., Nissenbaum A., Waisel Y..
Photosynthetic pathways and the ecological distribution of the Chenopodiaceae in Israel.
Oecologia.
(1981);
48
244-248
50
Ueno O..
Ultrastructural localization of photosynthetic and photorespiratory enzymes in epidermal, mesophyll, bundle sheath, and vascular bundle cells of the C4 dicot Amaranthus viridis .
Journal of Experimental Botany.
(2001);
52
1003-1013
51
von Caemmerer S., Farquhar G. D..
Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves.
Planta.
(1981);
153
376-387
52
von Caemmerer S., Furbank R. T..
The C4 pathway: an efficient CO2 pump.
Photosynthesis Research.
(2003);
77
191-207
53
Voznesenskaya E. V..
The ultrastructure of assimilating organs in some species of Chenopodiaceae family. I.
Botanicheskii Zhurnal.
(1976 a);
61
342-351
54
Voznesenskaya E. V..
Ultrastructure of assimilating organs of some species of the family Chenopodiaceae. II.
Botanicheskii Zhurnal.
(1976 b);
61
1546-1557
55
Voznesenskaya E. V., Franceschi V. R., Chuong S. D. X., Edwards G. E..
Functional characterization of phosphoenolpyruvate carboxykinase type C4 leaf anatomy: Immuno, cytochemical and ultrastructural analyses.
Annals of Botany.
(2006);
98
77-91
56
Voznesenskaya E. V., Franceschi V. R., Pyankov V. I., Edwards G. E..
Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae).
Journal of Experimental Botany.
(1999);
50
1779-1795
57
Voznesenskaya E. V., Gamaley Y. V..
The ultrastructural characteristics of leaf types with Kranz-anatomy.
Botanicheskii Zhurnal.
(1986);
71
1291-1307
58
Yoshimura Y., Kubota F., Ueno O..
Structural and biochemical bases of photorespiration in C4 plants: quantification of organelles and glycine decarboxylase.
Planta.
(2004);
220
307-317
G. E. Edwards
School of Biological Sciences Washington State University
Pullman, WA 99164-4236
USA
eMail: edwardsg@wsu.edu
Editor: R. C. Leegood