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Starch accumulation does not lead to feedback photosynthetic downregulation in girdled coffee branches under varying source-to-sink ratios

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Abstract

Key message

Leaves were forced to accumulate starch as much as possible but maintained relatively low soluble sugar levels with no evidence of photosynthetic feedback downregulation.

Abstract

Here, we examined whether the regulation of photosynthesis in coffee depends on sink activity or carbohydrate build-up in source leaves and how the coffee tree adjusts its photosynthetic performance and primary metabolism to varying source-to-sink ratios. We designed a field experiment by girdling coffee branches that were further manipulated by controlled defoliation and/or defruiting such that three highly varying source-to-sink ratios were created. Under markedly high source-to-sink ratios, photosynthesis rates were primarily limited by diffusional factors, and feedback downregulation contributed a maximum of 7% of the photosynthetic reduction. Such responses were accompanied by a relatively enormous capacity for starch accumulation coupled with the maintenance of low levels of soluble sugars. Chronic photoinhibition and photodamage could be avoided by increases in nonphotochemical energy dissipation, photorespiration and respiration rates, thus diminishing the excitation pressure on photosystems. Overall, the activities of key enzymes (and their transcript abundance) associated with carbon metabolism varied only marginally across treatments. Leaf metabolic adjustments were more evident under high sink demand conditions, and nitrogen metabolism was more affected than carbon metabolism. In conclusion, our results offer novel insights into the high coordination between the source supply and sink demand in coffee, with a minor role of photosynthetic downregulation even under dramatically low sink conditions.

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Abbreviations

AGPase:

ADP-glucose pyrophosphorylase

ALD:

Aldolase

CAST:

Clustering affinity search technique

DW:

Dry weight

ENO:

Enolase

ETR:

Apparent electron transport rate

FW:

Fresh weight

HK:

Hexokinase

HSS:

High source-to-sink ratio

ISS:

Intermediate source-to-sink ratio

LSS:

Low source-to-sink ratio

MeV:

MultiExperiment Viewer

NAD-GAP3DH:

NAD-dependent glyceraldehyde-3-phosphate dehydrogenase

NAD-MDH:

NAD-dependent malate dehydrogenase

NPQ:

Coefficient for non-photochemical quenching

PFK:

Phosphofructokinase

PGK:

Phosphoglycerate kinase

PPFD:

Photosynthetic photon flux density

qRT-PCR:

Quantitative real-time PCR

PS:

Photosystem

SPS:

Sucrose-phosphate synthase

SuSy:

Sucrose synthase

TCA:

Tricarboxylic acid

TPI:

Triose phosphate isomerase

A :

Net CO2 assimilation rate

C i :

Internal CO2 concentration

g m :

Mesophyll conductance

g s :

Stomatal conductance

F m :

Maximum fluorescence

F 0 :

Minimum fluorescence

Fm′:

Light-adapted maximum fluorescence

F s :

Steady-state fluorescence yield

Fv/Fm :

Variable-to-maximum fluorescence ratio

L b :

Biochemical limitation

L m :

Mesophyll limitation

L s :

Stomatal limitation

q p :

Coefficient for photochemical quenching

rbcS :

RuBisCO small subunit

R d :

Daytime respiration

R n :

Nocturnal respiration

Rp/Agross :

Photorespiration-to-gross photosynthesis ratio

V cmax :

Maximum apparent carboxylation capacity

Φ PSII :

Actual quantum yield of PSII electron transport

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Acknowledgements

Research fellowships that were granted by the National Council for Scientific and Technological Development (CNPq, Brazil) to W.L.A., A.N.N. and F.M.D. are gratefully acknowledged. We thank the scholarships that were granted by the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES), the Foundation for Research Assistance of Minas Gerais State, Brazil (FAPEMIG) and CNPq. We are also thankful to the Núcleo de Análises de Biomoléculas (NUBIOMOL) for providing the facilities to perform the metabolic profiling analyses.

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Authors and Affiliations

  1. Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Campus Viçosa, Avenida Peter Henry Rolfs, Viçosa, MG, 36570-900, Brazil

    Rodrigo T. Avila, Samuel C. V. Martins, Lílian M. V. P. Sanglard, Martielly S. dos Santos, Paulo E. Menezes-Silva, Kelly C. Detman, Matheus L. Sanglard, Amanda A. Cardoso, Leandro E. Morais & Fábio M. DaMatta

  2. Núcleo de Biomoléculas, Universidade Federal de Viçosa, Viçosa, MG, 36570-900, Brazil

    Camilo E. Vital

  3. Max Planck-Partner Group at the Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, 36570-900, Brazil

    Wagner L. Araújo & Adriano Nunes-Nesi

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  1. Rodrigo T. Avila
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  2. Samuel C. V. Martins
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Correspondence to Fábio M. DaMatta.

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Avila, R.T., Martins, S.C.V., Sanglard, L.M.V.P. et al. Starch accumulation does not lead to feedback photosynthetic downregulation in girdled coffee branches under varying source-to-sink ratios. Trees 34, 1–16 (2020). https://doi.org/10.1007/s00468-019-01893-8

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