C 4-like photosynthesis and the effects of leaf senescence on C 4-like physiology in Sesuvium sesuvioides (Aizoaceae)

Katharina Bohley, Till Schröder, Jürgen Kesselmeier, Martha Ludwig, Gudrun Kadereit

Research output: Contribution to journalArticle

Abstract

Sesuvium sesuvioides (Sesuvioideae, Aizoaceae) is a perennial, salt-tolerant herb distributed in flats, depressions, or disturbed habitats of southern Africa and the Cape Verdes. Based on carbon isotope values, it is considered a C 4 species, despite a relatively high ratio of mesophyll to bundle sheath cells (2.7:1) in the portulacelloid leaf anatomy. Using leaf anatomy, immunocytochemistry, gas exchange measurements, and enzyme activity assays, we sought to identify the biochemical subtype of C 4 photosynthesis used by S. sesuvioides and to explore the anatomical, physiological, and biochemical traits of young, mature, and senescing leaves, with the aim to elucidate the plasticity and possible limitations of the photosynthetic efficiency in this species. Assays indicated that S. sesuvioides employs the NADP-malic enzyme as the major decarboxylating enzyme. The activity of C 4 enzymes, however, declined as leaves aged, and the proportion of water storage tissue increased while air space decreased. These changes suggest a functional shift from photosynthesis to water storage in older leaves. Interestingly, S. sesuvioides demonstrated CO 2 compensation points ranging between C 4 and C 3-C 4 intermediate values, and immunocytochemistry revealed labeling of the Rubisco large subunit in mesophyll cells. We hypothesize that S. sesuvioides represents a young C 4 lineage with C 4-like photosynthesis in which C 3 and C 4 cycles are running simultaneously in the mesophyll.

Original languageEnglish
Pages (from-to)1553-1565
Number of pages14
JournalJournal of Experimental Botany
Volume70
Issue number5
DOIs
Publication statusPublished - 15 Feb 2019

Fingerprint

Sesuvium
Aizoaceae
Photosynthesis
physiology
photosynthesis
malate dehydrogenase (oxaloacetate-decarboxylating) (NADP+)
mesophyll
Anatomy
Immunohistochemistry
Mesophyll Cells
Carbon Isotopes
Ribulose-Bisphosphate Carboxylase
immunocytochemistry
Southern Africa
leaves
Water
Enzyme Assays
Enzymes
Carbon Monoxide
Ecosystem

Cite this

Bohley, Katharina ; Schröder, Till ; Kesselmeier, Jürgen ; Ludwig, Martha ; Kadereit, Gudrun. / C 4-like photosynthesis and the effects of leaf senescence on C 4-like physiology in Sesuvium sesuvioides (Aizoaceae). In: Journal of Experimental Botany. 2019 ; Vol. 70, No. 5. pp. 1553-1565.
@article{f656f329ee5b4a9699fd2a1e01c57bf7,
title = "C 4-like photosynthesis and the effects of leaf senescence on C 4-like physiology in Sesuvium sesuvioides (Aizoaceae)",
abstract = "Sesuvium sesuvioides (Sesuvioideae, Aizoaceae) is a perennial, salt-tolerant herb distributed in flats, depressions, or disturbed habitats of southern Africa and the Cape Verdes. Based on carbon isotope values, it is considered a C 4 species, despite a relatively high ratio of mesophyll to bundle sheath cells (2.7:1) in the portulacelloid leaf anatomy. Using leaf anatomy, immunocytochemistry, gas exchange measurements, and enzyme activity assays, we sought to identify the biochemical subtype of C 4 photosynthesis used by S. sesuvioides and to explore the anatomical, physiological, and biochemical traits of young, mature, and senescing leaves, with the aim to elucidate the plasticity and possible limitations of the photosynthetic efficiency in this species. Assays indicated that S. sesuvioides employs the NADP-malic enzyme as the major decarboxylating enzyme. The activity of C 4 enzymes, however, declined as leaves aged, and the proportion of water storage tissue increased while air space decreased. These changes suggest a functional shift from photosynthesis to water storage in older leaves. Interestingly, S. sesuvioides demonstrated CO 2 compensation points ranging between C 4 and C 3-C 4 intermediate values, and immunocytochemistry revealed labeling of the Rubisco large subunit in mesophyll cells. We hypothesize that S. sesuvioides represents a young C 4 lineage with C 4-like photosynthesis in which C 3 and C 4 cycles are running simultaneously in the mesophyll.",
keywords = "Aizoaceae, C 4 photosynthesis, C 4-like, carbon isotope values, immunolocalization of Rubisco and PEPC, portulacelloid leaf anatomy",
author = "Katharina Bohley and Till Schr{\"o}der and J{\"u}rgen Kesselmeier and Martha Ludwig and Gudrun Kadereit",
year = "2019",
month = "2",
day = "15",
doi = "10.1093/jxb/erz011",
language = "English",
volume = "70",
pages = "1553--1565",
journal = "Journal of Experimental Botany",
issn = "0022-0957",
publisher = "OXFORD UNIV PRESS UNITED KINGDOM",
number = "5",

}

C 4-like photosynthesis and the effects of leaf senescence on C 4-like physiology in Sesuvium sesuvioides (Aizoaceae). / Bohley, Katharina; Schröder, Till; Kesselmeier, Jürgen; Ludwig, Martha; Kadereit, Gudrun.

In: Journal of Experimental Botany, Vol. 70, No. 5, 15.02.2019, p. 1553-1565.

Research output: Contribution to journalArticle

TY - JOUR

T1 - C 4-like photosynthesis and the effects of leaf senescence on C 4-like physiology in Sesuvium sesuvioides (Aizoaceae)

AU - Bohley, Katharina

AU - Schröder, Till

AU - Kesselmeier, Jürgen

AU - Ludwig, Martha

AU - Kadereit, Gudrun

PY - 2019/2/15

Y1 - 2019/2/15

N2 - Sesuvium sesuvioides (Sesuvioideae, Aizoaceae) is a perennial, salt-tolerant herb distributed in flats, depressions, or disturbed habitats of southern Africa and the Cape Verdes. Based on carbon isotope values, it is considered a C 4 species, despite a relatively high ratio of mesophyll to bundle sheath cells (2.7:1) in the portulacelloid leaf anatomy. Using leaf anatomy, immunocytochemistry, gas exchange measurements, and enzyme activity assays, we sought to identify the biochemical subtype of C 4 photosynthesis used by S. sesuvioides and to explore the anatomical, physiological, and biochemical traits of young, mature, and senescing leaves, with the aim to elucidate the plasticity and possible limitations of the photosynthetic efficiency in this species. Assays indicated that S. sesuvioides employs the NADP-malic enzyme as the major decarboxylating enzyme. The activity of C 4 enzymes, however, declined as leaves aged, and the proportion of water storage tissue increased while air space decreased. These changes suggest a functional shift from photosynthesis to water storage in older leaves. Interestingly, S. sesuvioides demonstrated CO 2 compensation points ranging between C 4 and C 3-C 4 intermediate values, and immunocytochemistry revealed labeling of the Rubisco large subunit in mesophyll cells. We hypothesize that S. sesuvioides represents a young C 4 lineage with C 4-like photosynthesis in which C 3 and C 4 cycles are running simultaneously in the mesophyll.

AB - Sesuvium sesuvioides (Sesuvioideae, Aizoaceae) is a perennial, salt-tolerant herb distributed in flats, depressions, or disturbed habitats of southern Africa and the Cape Verdes. Based on carbon isotope values, it is considered a C 4 species, despite a relatively high ratio of mesophyll to bundle sheath cells (2.7:1) in the portulacelloid leaf anatomy. Using leaf anatomy, immunocytochemistry, gas exchange measurements, and enzyme activity assays, we sought to identify the biochemical subtype of C 4 photosynthesis used by S. sesuvioides and to explore the anatomical, physiological, and biochemical traits of young, mature, and senescing leaves, with the aim to elucidate the plasticity and possible limitations of the photosynthetic efficiency in this species. Assays indicated that S. sesuvioides employs the NADP-malic enzyme as the major decarboxylating enzyme. The activity of C 4 enzymes, however, declined as leaves aged, and the proportion of water storage tissue increased while air space decreased. These changes suggest a functional shift from photosynthesis to water storage in older leaves. Interestingly, S. sesuvioides demonstrated CO 2 compensation points ranging between C 4 and C 3-C 4 intermediate values, and immunocytochemistry revealed labeling of the Rubisco large subunit in mesophyll cells. We hypothesize that S. sesuvioides represents a young C 4 lineage with C 4-like photosynthesis in which C 3 and C 4 cycles are running simultaneously in the mesophyll.

KW - Aizoaceae

KW - C 4 photosynthesis

KW - C 4-like

KW - carbon isotope values

KW - immunolocalization of Rubisco and PEPC

KW - portulacelloid leaf anatomy

UR - http://www.scopus.com/inward/record.url?scp=85062835173&partnerID=8YFLogxK

U2 - 10.1093/jxb/erz011

DO - 10.1093/jxb/erz011

M3 - Article

VL - 70

SP - 1553

EP - 1565

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

SN - 0022-0957

IS - 5

ER -