Alternative Oxidase (AOX) Senses Stress Levels to Coordinate Auxin-Induced Reprogramming From Seed Germination to Somatic Embryogenesis—A Role Relevant for Seed Vigor Prediction and Plant Robustness

Gunasekaran Mohanapriya, Revuru Bharadwaj, Carlos Noceda, José Hélio Costa, Sarma Rajeev Kumar, Ramalingam Sathishkumar*, Karine Leitão Lima Thiers, Elisete Santos Macedo, Sofia Silva, Paolo Annicchiarico, Steven P.C. Groot, Jan Kodde, Aprajita Kumari, Kapuganti Jagadis Gupta, Birgit Arnholdt-Schmitt

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Somatic embryogenesis (SE) is the most striking and prominent example of plant plasticity upon severe stress. Inducing immature carrot seeds perform SE as substitute to germination by auxin treatment can be seen as switch between stress levels associated to morphophysiological plasticity. This experimental system is highly powerful to explore stress response factors that mediate the metabolic switch between cell and tissue identities. Developmental plasticity per se is an emerging trait for in vitro systems and crop improvement. It is supposed to underlie multi-stress tolerance. High plasticity can protect plants throughout life cycles against variable abiotic and biotic conditions. We provide proof of concepts for the existing hypothesis that alternative oxidase (AOX) can be relevant for developmental plasticity and be associated to yield stability. Our perspective on AOX as relevant coordinator of cell reprogramming is supported by real-time polymerase chain reaction (PCR) analyses and gross metabolism data from calorespirometry complemented by SHAM-inhibitor studies on primed, elevated partial pressure of oxygen (EPPO)–stressed, and endophyte-treated seeds. In silico studies on public experimental data from diverse species strengthen generality of our insights. Finally, we highlight ready-to-use concepts for plant selection and optimizing in vivo and in vitro propagation that do not require further details on molecular physiology and metabolism. This is demonstrated by applying our research & technology concepts to pea genotypes with differential yield performance in multilocation fields and chickpea types known for differential robustness in the field. By using these concepts and tools appropriately, also other marker candidates than AOX and complex genomics data can be efficiently validated for prebreeding and seed vigor prediction.

Original languageEnglish
Article number1134
JournalFrontiers in Plant Science
Volume10
DOIs
Publication statusPublished - 20 Sep 2019

Fingerprint

vigor
auxins
seed germination
somatic embryogenesis
prediction
seeds
metabolism
endophytes
stress tolerance
carrots
life cycle (organisms)
stress response
peas
quantitative polymerase chain reaction
physiology
immatures
cells
germination
genomics
oxygen

Keywords

  • developmental plasticity
  • endophytes
  • environmental stress
  • metabolic biomarker
  • plant performance prediction
  • seed technology

Cite this

Mohanapriya, Gunasekaran ; Bharadwaj, Revuru ; Noceda, Carlos ; Costa, José Hélio ; Kumar, Sarma Rajeev ; Sathishkumar, Ramalingam ; Thiers, Karine Leitão Lima ; Santos Macedo, Elisete ; Silva, Sofia ; Annicchiarico, Paolo ; Groot, Steven P.C. ; Kodde, Jan ; Kumari, Aprajita ; Gupta, Kapuganti Jagadis ; Arnholdt-Schmitt, Birgit. / Alternative Oxidase (AOX) Senses Stress Levels to Coordinate Auxin-Induced Reprogramming From Seed Germination to Somatic Embryogenesis—A Role Relevant for Seed Vigor Prediction and Plant Robustness. In: Frontiers in Plant Science. 2019 ; Vol. 10.
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abstract = "Somatic embryogenesis (SE) is the most striking and prominent example of plant plasticity upon severe stress. Inducing immature carrot seeds perform SE as substitute to germination by auxin treatment can be seen as switch between stress levels associated to morphophysiological plasticity. This experimental system is highly powerful to explore stress response factors that mediate the metabolic switch between cell and tissue identities. Developmental plasticity per se is an emerging trait for in vitro systems and crop improvement. It is supposed to underlie multi-stress tolerance. High plasticity can protect plants throughout life cycles against variable abiotic and biotic conditions. We provide proof of concepts for the existing hypothesis that alternative oxidase (AOX) can be relevant for developmental plasticity and be associated to yield stability. Our perspective on AOX as relevant coordinator of cell reprogramming is supported by real-time polymerase chain reaction (PCR) analyses and gross metabolism data from calorespirometry complemented by SHAM-inhibitor studies on primed, elevated partial pressure of oxygen (EPPO)–stressed, and endophyte-treated seeds. In silico studies on public experimental data from diverse species strengthen generality of our insights. Finally, we highlight ready-to-use concepts for plant selection and optimizing in vivo and in vitro propagation that do not require further details on molecular physiology and metabolism. This is demonstrated by applying our research & technology concepts to pea genotypes with differential yield performance in multilocation fields and chickpea types known for differential robustness in the field. By using these concepts and tools appropriately, also other marker candidates than AOX and complex genomics data can be efficiently validated for prebreeding and seed vigor prediction.",
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Mohanapriya, G, Bharadwaj, R, Noceda, C, Costa, JH, Kumar, SR, Sathishkumar, R, Thiers, KLL, Santos Macedo, E, Silva, S, Annicchiarico, P, Groot, SPC, Kodde, J, Kumari, A, Gupta, KJ & Arnholdt-Schmitt, B 2019, 'Alternative Oxidase (AOX) Senses Stress Levels to Coordinate Auxin-Induced Reprogramming From Seed Germination to Somatic Embryogenesis—A Role Relevant for Seed Vigor Prediction and Plant Robustness', Frontiers in Plant Science, vol. 10, 1134. https://doi.org/10.3389/fpls.2019.01134

Alternative Oxidase (AOX) Senses Stress Levels to Coordinate Auxin-Induced Reprogramming From Seed Germination to Somatic Embryogenesis—A Role Relevant for Seed Vigor Prediction and Plant Robustness. / Mohanapriya, Gunasekaran; Bharadwaj, Revuru; Noceda, Carlos; Costa, José Hélio; Kumar, Sarma Rajeev; Sathishkumar, Ramalingam; Thiers, Karine Leitão Lima; Santos Macedo, Elisete; Silva, Sofia; Annicchiarico, Paolo; Groot, Steven P.C.; Kodde, Jan; Kumari, Aprajita; Gupta, Kapuganti Jagadis; Arnholdt-Schmitt, Birgit.

In: Frontiers in Plant Science, Vol. 10, 1134, 20.09.2019.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - Alternative Oxidase (AOX) Senses Stress Levels to Coordinate Auxin-Induced Reprogramming From Seed Germination to Somatic Embryogenesis—A Role Relevant for Seed Vigor Prediction and Plant Robustness

AU - Mohanapriya, Gunasekaran

AU - Bharadwaj, Revuru

AU - Noceda, Carlos

AU - Costa, José Hélio

AU - Kumar, Sarma Rajeev

AU - Sathishkumar, Ramalingam

AU - Thiers, Karine Leitão Lima

AU - Santos Macedo, Elisete

AU - Silva, Sofia

AU - Annicchiarico, Paolo

AU - Groot, Steven P.C.

AU - Kodde, Jan

AU - Kumari, Aprajita

AU - Gupta, Kapuganti Jagadis

AU - Arnholdt-Schmitt, Birgit

PY - 2019/9/20

Y1 - 2019/9/20

N2 - Somatic embryogenesis (SE) is the most striking and prominent example of plant plasticity upon severe stress. Inducing immature carrot seeds perform SE as substitute to germination by auxin treatment can be seen as switch between stress levels associated to morphophysiological plasticity. This experimental system is highly powerful to explore stress response factors that mediate the metabolic switch between cell and tissue identities. Developmental plasticity per se is an emerging trait for in vitro systems and crop improvement. It is supposed to underlie multi-stress tolerance. High plasticity can protect plants throughout life cycles against variable abiotic and biotic conditions. We provide proof of concepts for the existing hypothesis that alternative oxidase (AOX) can be relevant for developmental plasticity and be associated to yield stability. Our perspective on AOX as relevant coordinator of cell reprogramming is supported by real-time polymerase chain reaction (PCR) analyses and gross metabolism data from calorespirometry complemented by SHAM-inhibitor studies on primed, elevated partial pressure of oxygen (EPPO)–stressed, and endophyte-treated seeds. In silico studies on public experimental data from diverse species strengthen generality of our insights. Finally, we highlight ready-to-use concepts for plant selection and optimizing in vivo and in vitro propagation that do not require further details on molecular physiology and metabolism. This is demonstrated by applying our research & technology concepts to pea genotypes with differential yield performance in multilocation fields and chickpea types known for differential robustness in the field. By using these concepts and tools appropriately, also other marker candidates than AOX and complex genomics data can be efficiently validated for prebreeding and seed vigor prediction.

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KW - developmental plasticity

KW - endophytes

KW - environmental stress

KW - metabolic biomarker

KW - plant performance prediction

KW - seed technology

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DO - 10.3389/fpls.2019.01134

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JO - Frontiers in Plant Science

JF - Frontiers in Plant Science

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