Journal Article

Significant involvement of PEP-CK in carbon assimilation of C<sub>4</sub> eudicots

Riyadh Muhaidat and Athena D. McKown

in Annals of Botany

Published on behalf of The Annals of Botany Company

Volume 111, issue 4, pages 577-589
Published in print April 2013 | ISSN: 0305-7364
Published online February 2013 | e-ISSN: 1095-8290 | DOI:
Significant involvement of PEP-CK in carbon assimilation of C4 eudicots

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  • Ecology and Conservation
  • Evolutionary Biology
  • Plant Sciences and Forestry


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Background and Aims

C4 eudicot species are classified into biochemical sub-types of C4 photosynthesis based on the principal decarboxylating enzyme. Two sub-types are known, NADP-malic enzyme (ME) and NAD-ME; however, evidence for the occurrence or involvement of the third sub-type (phosphoenolpyruvate carboxykinase; PEP-CK) is emerging. In this study, the presence and activity of PEP-CK in C4 eudicot species of Trianthema and Zaleya (Sesuvioideae, Aizoaceae) is clarified through analysis of key anatomical features and C4 photosynthetic enzymes.


Three C4 species (T. portulacastrum, T. sheilae and Z. pentandra) were examined with light and transmission electron microscopy for leaf structural properties. Activities and immunolocalizations of C4 enzymes were measured for biochemical characteristics.

Key Results

Leaves of each species possess atriplicoid-type Kranz anatomy, but differ in ultrastructural features. Bundle sheath organelles are centripetal in T. portulacastrum and Z. pentandra, and centrifugal in T. sheilae. Bundle sheath chloroplasts in T. portulacastrum are almost agranal, whereas mesophyll counterparts have grana. Both T. sheilae and Z. pentandra are similar, where bundle sheath chloroplasts contain well-developed grana while mesophyll chloroplasts are grana deficient. Cell wall thickness is significantly greater in T. sheilae than in the other species. Biochemically, T. portulacastrum is NADP-ME, while T. sheilae and Z. pentandra are NAD-ME. Both T. portulacastrum and Z. pentandra exhibit considerable PEP-CK activity, and immunolocalization studies show dense and specific compartmentation of PEP-CK in these species, consistent with high PEP-CK enzyme activity.


Involvement of PEP-CK in C4 NADP-ME T. portulacastrum and NAD-ME Z. petandra occurs irrespective of biochemical sub-type, or the position of bundle sheath chloroplasts. Ultrastructural traits, including numbers of bundle sheath peroxisomes and mesophyll chloroplasts, and degree of grana development in bundle sheath chloroplasts, coincide more directly with PEP-CK recruitment. Discovery of high PEP-CK activity in C4 Sesuvioideae species offers a unique opportunity for evaluating PEP-CK expression and suggests the possibility that PEP-CK recruitment may exist elsewhere in C4 eudicots.

Keywords: Aizoaceae; C4 photosynthesis; granal development; Kranz anatomy; NADP-ME sub-type; NAD-ME sub-type; PEP-CK sub-type; Sesuvioideae; thylakoid; Trianthema portulacastrum; Trianthema sheilae; Zaleya pentandra

Journal Article.  8653 words.  Illustrated.

Subjects: Ecology and Conservation ; Evolutionary Biology ; Plant Sciences and Forestry

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