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Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass.

ABSTRACT: C₄ photosynthesis is thought to have evolved via intermediate stages, with changes towards the C₄ phenotype gradually enhancing photosynthetic performance. This hypothesis is widely supported by modelling studies, but experimental tests are missing. Mixing of C₄ components to generate artificial intermediates can be achieved via crossing, and the grass Alloteropsis semialata represents an outstanding study system since it includes C₄ and non-C₄ populations. Here, we analyse F1 hybrids between C₃ and C₄ , and C₃ +C₄ and C₄ genotypes to determine whether the acquisition of C₄ characteristics increases photosynthetic performance. The hybrids have leaf anatomical characters and C₄ gene expression profiles that are largely intermediate between those of their parents. Carbon isotope ratios are similarly intermediate, which suggests that a partial C₄ cycle coexists with C₃ carbon fixation in the hybrids. This partial C₄ phenotype is associated with C₄ -like photosynthetic efficiency in C₃ +C₄ × C₄ , but not in C₃ × C₄ hybrids, which are overall less efficient than both parents. Our results support the hypothesis that the photosynthetic gains from the upregulation of C₄ characteristics depend on coordinated changes in anatomy and biochemistry. The order of acquisition of C₄ components is thus constrained, with C₃ +C₄ species providing an essential step for C₄ evolution.

SUBMITTER: Bianconi ME

PROVIDER: S-EPMC9314825 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Upregulation of C4 characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass.

Bianconi Matheus E ME Sotelo Graciela G Curran Emma V EV Milenkovic Vanja V Samaritani Emanuela E Dunning Luke T LT Bertolino Lígia T LT Osborne Colin P CP Christin Pascal-Antoine PA

Plant, cell & environment 20220310 5

C4 photosynthesis is thought to have evolved via intermediate stages, with changes towards the C4 phenotype gradually enhancing photosynthetic performance. This hypothesis is widely supported by modelling studies, but experimental tests are missing. Mixing of C4 components to generate artificial intermediates can be achieved via crossing, and the grass Alloteropsis semialata represents an outstanding study system since it includes C4 and non-C4</s ...[more]

PMID: 35201618

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Project description:Numerous studies have shown that temperate and boreal forests are limited by nitrogen (N) availability. However, few studies have provided a detailed account of how carbon (C) acquisition of such forests reacts to increasing N supply. We combined measurements of needle-scale biochemical photosynthetic capacities and continuous observations of shoot-scale photosynthetic performance from several canopy positions with simple mechanistic modeling to evaluate the photosynthetic responses of mature N-poor boreal Pinus sylvestris to N fertilization. The measurements were carried out in August 2013 on 90-year-old pine trees growing at Rosinedalsheden research site in northern Sweden. In spite of a nearly doubling of needle N content in response to the fertilization, no effect on the long-term shoot-scale C uptake was recorded. This lack of N-effect was due to strong light limitation of photosynthesis in all investigated canopy positions. The effect of greater N availability on needle photosynthetic capacities was also constrained by development of foliar phosphorus (P) deficiency following N addition. Thus, P deficiency and accumulation of N in arginine appeared to contribute toward lower shoot-scale nitrogen-use efficiency in the fertilized trees, thereby additionally constraining tree-scale responses to increasing N availability. On the whole our study suggests that the C uptake response of the studied N-poor boreal P. sylvestris stand to enhanced N availability is constrained by the efficiency with which the additional N is utilized. This efficiency, in turn, depends on the ability of the trees to use the greater N availability for additional light capture. For stands that have not reached canopy closure, increase in leaf area following N fertilization would be the most effective way for improving light capture and C uptake while for mature stands an increased leaf area may have a rather limited effect on light capture owing to increased self-shading. This raises the question if N limitation in boreal forests acts primarily by constraining growth of young stands while the commonly recorded increase in stem growth of mature stands following N addition is primarily the result of altered allocation and only to a limited extent the result of increased stand C-capture.

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Upregulation of C₄ characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass.

Publications

Upregulation of C<sub>4</sub> characteristics does not consistently improve photosynthetic performance in intraspecific hybrids of a grass.

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