Predicting Biomass Production from Plant Robustness and Germination Efficiency by Calorespirometry

  • Birgit Arnholdt-Schmitt
  • Gunasekaran Mohanapriya
  • Ramalingam Sathishkumar
  • Elisete Santos Macedo
  • José Hélio Costa


Respiration traits allow calculating temperature-dependent carbon use efficiency and can serve as biomarkers for the prediction of growth and biomass formation. While photosynthesis is responsible for capturing CO2, respiration critically manages the destiny of structurally integrated CO2 by regulating the use of energy and substances. The efficient interplay of cytochrome and alternative respiration pathways determines plant performance upon permanently changing and interacting abiotic and biotic environment. Thus, respiration traits are central for high biomass production and yield stability based on multi-stress tolerance. Hence, calorespirometry is a useful functional tool for pre-breeding that can discriminate plants based on genetic differences in respiration traits. Although it was earlier suggested that the methodology could be valuable in breeding programs to improve temperature-dependent growth performance, this concept had never been applied in global breeding on biomass production. This predictive tool can be applied as an efficient mean (1) to identify differences in germination efficiency among genotypes or through management practice in seed technology, (2) to select plants in conventional breeding, and (3) to identify relevant genomics-based functional markers for temperature-dependent multi-stress tolerance and yield stability. From respiration-related genes, alternative oxidase is a promising candidate for functional marker development. It relates to both germination efficiency and plant robustness linked to biomass yield stability.


Calorespirometry Alternative respiration Germination efficiency Genomics Functional marker development 



The authors thank the Indian-Portugal Bilateral Cooperation Programme (2013–2015), funded by “Fundação para a Ciência e Tecnologia” (FCT), Portugal, and the Department of Science and Technology of the Indian Government for support to the academic cooperation and researchers mobility.


  1. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11(10):R106.
  2. Arnholdt-Schmitt B (1995) Physiological aspects of genome variability in tissue culture II. Growth phase – dependent quantitative variability of repetitive BstNI fragments of primary cultures of Daucus carota L. Theor Appl Gen 91(5):816–823. Google Scholar
  3. Arnholdt-Schmitt B (1999) On the physiology of yield production in carrots – implications for breeding towards nutrient efficiency. Gartenbauwissenschaft 64(1):26–32. ISSN: 0016-478XGoogle Scholar
  4. Arnholdt-Schmitt B (2004) Stress-induced cell reprogramming. A role for global genome regulation? Plant Physiol 136(1):2579–2586CrossRefGoogle Scholar
  5. Arnholdt-Schmitt B (2005a) Functional markers and a systemic strategy: convergency between plant breeding, plant nutrition and molecular biology. Plant Physiol Biochem 43(9):817–820. CrossRefGoogle Scholar
  6. Arnholdt-Schmitt B (2005b) Efficient cell reprogramming as a target for functional marker strategies? Towards new perspectives in applied plant nutrition research. J Plant Nutr Soil Sci 168(4):617–624. CrossRefGoogle Scholar
  7. Arnholdt-Schmitt B (2017) Respiration traits as novel markers for plant robustness under the threat of climate change – a protocol for validation. In: Walker John M, Gupta KJ (ed) Methods in molecular biology, Springer protocols and hard cover by Humana Press. ISSN: 1064-3745Google Scholar
  8. Arnholdt-Schmitt B, Kumar Patil V (2017) Studying individual plant AOX gene functionality in early growth regulation – a new approach. In: Walker, John M (chief-eds) Gupta KJ (eds) Methods in molecular biology: plant respiration & internal oxygen: methods and protocols, Springer protocols and hard cover by Humana Press. ISSN: 1064–3745Google Scholar
  9. Arnholdt-Schmitt B, Costa JH, De Melo DF (2006) AOX – a functional marker for efficient cell reprogramming under stress? Trends Plant Sci 11(6):281–287. CrossRefGoogle Scholar
  10. Arnholdt-Schmitt B, Valadas V, Döring M (2016) Functional marker development is challenged by the ubiquity of endophytes – a practical perspective. Brief Funct Genomics 15:16–21.
  11. Arnholdt-Schmitt B, Ragonezi C, Cardoso H (2015) A central role of mitochondria for stress-induced somatic embryogenesis? In: Germanà MA, Lambardi M (eds) In vitro plant embryogenesis in higher plants, series ‘Methods in Molecular Biology’, Springer-Humana PressGoogle Scholar
  12. Arnholdt-Schmitt B, Hansen LD, Nogales A (2016) Calorespirometry, oxygen isotope analysis and functional-marker-assisted selection (‘CalOxy-FMAS’) for genotype screening: a novel concept and tool kit for predicting stable plant growth performance and functional marker identification. Brief Funct Genomics 15(1):10–15. Google Scholar
  13. Bonner WD (1973) Mitochondria and plant respiration. Phytochemistry 3:221–261. cited in Yentur and Leopold (1976)Google Scholar
  14. Botha FC, Potgieter GP, Botha AM (1992) Respiratory metabolism and gene expression during seed germination. Plant Growth Regul 11(3):211–224. CrossRefGoogle Scholar
  15. Campos MD, Nogales A, Cardoso HG, Kumar SR, Sathishkumar R, Arnholdt-Schmitt B (2016) Stress-induced accumulation of DcAOX1 and DcAOX2a transcripts coincides with critical time point for structural biomass prediction in carrot primary cultures (Daucus carota L.). Front Genet 7:1.
  16. Cardoso HG, Arnholdt-Schmitt B (2013) Functional marker development across species in selected trait. In: Lubberstedt T, Varshney RK (eds) Diagnostics in plant breeding. Springer, Dordrecht, pp 467–515. CrossRefGoogle Scholar
  17. Clifton R, Millar AH, Whelan J (2006) Alternative oxidase in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim Biophys Acta 1757(7):730–741. CrossRefGoogle Scholar
  18. Costa JH, Cardoso HG, Campos MD, Zavattieri A, Frederico AM, De Melo DF, Arnholdt-Schmitt B (2009) Daucus carota L.- an old model for cell reprogramming gains new importance through a novel expansion pattern of alternative oxidase (AOX) genes. Plant Physiol Biochem 47(8):753–759. [Corrigendum to “Daucus carota L.- an old model for cell reprogramming gains new importance through a novel expansion pattern of alternative oxidase (AOX) genes. Plant Physiol Biochem 85:114.” doi:]
  19. Costa JH, McDonald A, Arnholdt-Schmitt B, De Melo DF (2014) A classification scheme for alternative oxidases reveals the taxonomic distribution and evolutionary history of the enzyme in angiosperms. Mitochondrion 19:172–183. CrossRefGoogle Scholar
  20. Costa JH, Santos CP, Lima BS, Netto ANM, Saraiva KDC, Arnholdt-Schmitt B (2017) In silico identification of alternative oxidase 2 (AOX2) in monocots: an evolutionary scenario. J Plant Physiol:58–63.
  21. De Souza A, Garcí D, Sueiro L, Gilart F, Porras E, Licea L (2006) Pre-sowing magnetic treatments of tomato seeds increase the growth and yield of plants. Bioelectromagnetics 27(4):247–257. CrossRefGoogle Scholar
  22. De Souza A, García D, Sueiro L, Gilart F (2014) Improvement of the seed germination, growth and yield of onion plants by extremely low frequency non-uniform magnetic fields. Sci Hortic 176:63–69.
  23. De Sousa AS, Paparella S, Dondi D, Bentivoglio A, Carbonera D, Balestrazzi A (2016) Physical methods for seed invigoration: advantages and challenges in seed technology. Front Plant Sci 7:646. CrossRefGoogle Scholar
  24. Dinakar C, Vishwakarma A, Raghavendra AS, Padmasree K (2016) Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems. Front Plant Sci 7:68. CrossRefGoogle Scholar
  25. Esashi Y, Sakai Y, Ushizawa R (1981) Cyanide-sensitive and cyanide-resistant respiration in the germination of cocklebur seeds. Plant Physiol 67(3):503–508. CrossRefGoogle Scholar
  26. Guy RD, Berry JA, Fogel ML, Hoering TC (1989) Differential fractionation of oxygen isotopes by cyanide-resistant and cyanide-sensitive respiration in plants. Planta 177(4):483–491. CrossRefGoogle Scholar
  27. Hansen LD, Hopkin MS, Criddle RS (1997) Plant calorimetry: a window to plant physiology and ecology. Thermochim Acta 300:183–197. CrossRefGoogle Scholar
  28. Hansen LD, Criddle RS, Smith BN (2005) Calorespirometry in plant biology. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem, Advaneces in Photosynthesis and Respiration. Springer, Dordrecht, pp 17–30CrossRefGoogle Scholar
  29. Hansen LD, Thomas NR, Arnholdt-Schmitt B (2009) Temperature responses of substrate carbon conversion efficiencies and growth rates of plant tissues. Physiol Plant 137(4):446–458. CrossRefGoogle Scholar
  30. Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA (2016) A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J 88(6):1058–1070.
  31. Matwijczuk A, Kornarzynski K, Pietruszewski S (2011) Effect of magnetic field on seed germination and seedling growth of sunflower. Int Agrophys 26:271–278. Google Scholar
  32. Mercy L, Lucic-Mercy E, Nogales A, Poghosyan A, Schneider C, Arnholdt-Schmitt B (2017) A functional approach towards understanding the role of the mitochondrial respiratory chain in an endomycorrhizal symbiosis. Front Plant Sci 8:417. CrossRefGoogle Scholar
  33. Momen B, Anderson PD, Sullivan JH, Helms JA (2004) A multivariate statistical approach to predicting mature tree performance based on seedling characteristics. New For 27:303–313.
  34. Mühleisen J, Piepho HP, Maurer HP, Longin CF, Reif JC (2014) Yield stability of hybrids versus lines in wheat, barley, and triticale. Theor Appl Genet 127(2):309–316. CrossRefGoogle Scholar
  35. Nogales A, Muñoz-Sanhueza L, Hansen LD, Arnholdt-Schmitt B (2013) Calorespirometry as a tool for studying temperature response in carrot (Daucus carota L). Eng Life Sci 13(6):541–548.
  36. Nogales A, Munoz-Sanhueza L, Hansen LD, Arnholdt-Schmitt B (2014) Phenotyping carrot (Daucus carota L.) for yield-determining temperature response by calorespirometry. Planta 241(2):525–538.
  37. Nogales A, Nobre T, Valadas V, Ragonezi C, Döring M, Polidoros A, Arnholdt-Schmitt B (2016) Can functional hologenomics aid tackling current challenges in plant breeding? Brief Funct Genomics 15:288–297.
  38. Paparella S, De Sousa AS, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the art and new perspectives. Plant Cell Rep 34:1281–1293. CrossRefGoogle Scholar
  39. Parsons RF (2012) Incidence and ecology of very fast germination. Seed Sci Res 22(3):161–167. CrossRefGoogle Scholar
  40. Paszkiewicz G, Gualberto JM, Benamar A, Macherel D, Logan DC (2017) Arabidopsis seed mitochondria are bioenergetically active immediately upon imbibitions and specialize via biogenesis in preparation for autotrophic growth. Plant Cell 29(1):109–128. CrossRefGoogle Scholar
  41. Ribas-Carbo M, Robinson SA, Giles L (2005) The application of the oxygen-isotope technique to assess respiratory pathway partitioning. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem, advances in photosynthesis and respiration. Springer, Dordrecht, pp 17–30. ISSN: 978-1-4020-3589-0Google Scholar
  42. Saisho D, Nakazono M, Lee KH, Tsutsumi N, Akita S, Hirai A (2001) The gene for alternative oxidase-2 (AOX2) from Arabidopsis Thaliana consists of five exons unlike other AOX genes and is transcribed at an early stage during germination. Genes Genet Syst 76:89–97.
  43. Sieger SM, Kristensen BK, Robson CA, Amirsadeghi S, Eng EW, Abdel-Mesih A, Moller IM, Vanlerberghe GC (2005) The role of alternative oxidase in modulating carbon use efficiency and growth during macronutrient stress in tobacco cells. J Exp Bot 56(416):1499–1515. CrossRefGoogle Scholar
  44. Taylor DK, Rank DR, Keiser DR, Smith BN, Criddle RS, Hansen LD (1998) Modelling temperature effects growth-respiration relations of maize. Plant Cell Environ 21(11):1143–1151. CrossRefGoogle Scholar
  45. Tian Y, Guan B, Zhou D, Yu J, Li G, Lou Y (2014) Responses of seed germination, seedling growth, and seed yield traits to seed pretreatment in maize (Zea mays L.). Sci World J 2014:834630.
  46. Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14(4):6805–6847. CrossRefGoogle Scholar
  47. Velada I, Cardoso HG, Ragonezi C, Nogales A, Ferreira A, Valadas V, Arnholdt-Schmitt B (2016) Alternative oxidase gene family in Hypericum perforatum L.: characterization and expression at the post-germinative phase. Front Plant Sci 7:1043.
  48. Wang Z, Chen F, Li X, Cao H, Ding M, Zhang C, Zuo J, Xu C, Xu J, Deng X, Xiang Y, Soppe WJJ, Liu Y (2016) Arabidopsis seed germination speed is controlled by SNL histone deacetylase-binding factor-mediated regulation of AUX1. Nat Commun 7:13414.
  49. Yentur S, Leopold AC (1976) Respiratory transition during seed germination. Plant Physiol 57(2):274–276. CrossRefGoogle Scholar
  50. Yuan W, Flowers JM, Sahraie DJ, Purugganan MD (2016a) Cryptic genetic variation for Arabidopsis thaliana seed germination speed in a novel salt stress environment. G3 (Bethesda) 6(10):3129–3138.
  51. Yuan W, Flowers JM, Sahraie DJ, Ehrenreich IM, Purugganan MD (2016b) Extreme QTL mapping of germination speed in Arabidopsis thaliana. Mol Ecol 2(17):4177–4196. CrossRefGoogle Scholar

Copyright information

© Springer (India) Pvt. Ltd. 2018

Authors and Affiliations

  • Birgit Arnholdt-Schmitt
    • 1
    • 2
    • 3
  • Gunasekaran Mohanapriya
    • 4
  • Ramalingam Sathishkumar
    • 4
  • Elisete Santos Macedo
    • 1
    • 2
  • José Hélio Costa
    • 3
  1. 1.Functional Cell Reprogramming and Organism Plasticity (FunCrop), EU Marie Curie Chair, ICAAMUniversity of ÉvoraÉvoraPortugal
  2. 2.Science and Technology Park Alentejo (PACT)ÉvoraPortugal
  3. 3.Functional Genomics and Bioinformatics, Department of Biochemistry and Molecular BiologyFederal University of CearáFortalezaBrazil
  4. 4.Plant Genetic Engineering Laboratory, Department of BiotechnologyBharathiar UniversityCoimbatoreIndia

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