Elucidating drought responsive networks in tef (Eragrostis tef) using phenomic and metabolomic approaches.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Jan 2022
Jan 2022
Historique:
revised:
28
10
2021
received:
10
09
2021
accepted:
10
11
2021
pubmed:
19
11
2021
medline:
26
2
2022
entrez:
18
11
2021
Statut:
ppublish
Résumé
Drought is a major abiotic stress that limits crop productivity and is driving the need to introduce new tolerant crops with better economic yield. Tef (Eragrostis tef) is a neglected (orphan) Ethiopian warm-season annual gluten-free cereal with high nutritional and health benefits. Further, tef is resilient to environmental challenges such as drought, but the adaptive mechanisms remain poorly understood. In this study, metabolic changes associated with drought response in 11 tef accessions were identified using phenomic and metabolomic approaches under controlled conditions. Computerized image analysis of droughted plants indicated reductions in leaf area and green pigments compared with controls. Metabolite profiling based on flow-infusion electrospray-high-resolution mass spectroscopy (FIE-HRMS) showed drought associated changes in flavonoid, phenylpropanoid biosynthesis, sugar metabolism, valine, leucine and isoleucine biosynthesis, and pentose phosphate pathways. Flavonoid associated metabolites and TCA intermediates were lower in the drought group, whereas most of the stress-responsive amino acids and sugars were elevated. Interestingly, after drought treatment, one accession Enatite (Ent) exhibited a significantly higher plant area than the others, and greater accumulation of flavonoids, amino acids (serine and glycine), sugars (ribose, myo-inositol), and fatty acids. The increased accumulation of these metabolites could explain the increased tolerance to drought in Ent compared with other accessions. This is the first time a non-targeted metabolomics approach has been applied in tef, and our results provide a framework for a better understanding of the tef metabolome during drought stress that will help to identify traits to improve this understudied potential crop.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13597Subventions
Organisme : European Commission Marie Skłodowska-Curie Individual Fellowship (Horizon 2020)
ID : 842118 SUPERTEFF
Informations de copyright
© 2021 Scandinavian Plant Physiology Society.
Références
Abraha, M.T., Shimelis, H.A., Laing, M.D. & Assefa, K. (2017) Selection of drought-tolerant tef (Eragrostis tef) genotypes using drought tolerance indices. South African Journal of Plant and Soil, 34(4), 291-300.
Abraha, M.T., Shimelis, H., Laing, M., Assefa, K. & Tuberosa, R. (2018) Gene action controlling yield and yield-related traits among tef (Eragrostis tef [Zucc.] Trotter) populations under drought-stressed and nonstressed conditions. Plant Breeding, 137(4), 585-597.
Allwood, W.J., Ellis, D.I., Heald, J.K., Goodacre, R. & Mur, L.A. (2006) Metabolomic approaches reveal that phosphatidic and phosphatidyl glycerol phospholipids are major discriminatory non-polar metabolites in responses by Brachypodium distachyon to challenge by Magnaporthe grisea. The Plant Journal, 46(3), 351-368.
Araya, A., Stroosnijder, L., Girmay, G. & Keesstra, S.D. (2011) Crop coefficient, yield response to water stress and water productivity of teff (Eragrostis tef (Zucc.)). Agricultural Water Management, 98(5), 775-783.
Assefa, K., Cannarozzi, G., Girma, D., Kamies, R., Chanyalew, S., Plaza-Wathrich, S. et al. (2015) Genetic diversity in tef [Eragrostis tef (Zucc.) Trotter]. Frontiers in Plant Science, 6, 177.
Bowne, J.B., Erwin, T.A., Juttner, J., Schnurbusch, T., Langridge, P., Bacic, A. et al. (2012) Drought responses of leaf tissues from wheat cultivars of differing drought tolerance at the metabolite level. Molecular Plant, 5(2), 418-429.
Cao, M., Fraser, K., Jones, C., Stewart, A., Lyons, T., Faville, M. et al. (2017) Untargeted metabotyping lolium perenne reveals population-level variation in plant flavonoids and alkaloids. Frontiers in Plant Science, 8(133), 1-12.
Carrizo, I.M., López Colomba, E., Tommasino, E., Carloni, E., Bollati, G., & Grunberg, K. (2021) Contrasting adaptive responses to cope with drought stress and recovery in Cenchrus ciliaris L. and their implications for tissue lignification. Physiologia Plantarum, 172, 762-779. https://doi.org/10.1111/ppl.13274
Chanyalew, S., Ferede, S., Damte, T., Fikre, T., Genet, Y., Kebede, W. et al. (2019) Significance and prospects of an orphan crop tef. Planta, 250(3), 753-767.
Chanyalew, S., Kebede, W., Fikire, T., Genet, Y., Jifar, H., Demissie, M. et al. (2021) Tef breeding manual. Debre Zeit, Ethiopia: National Tef Research Program; Debre Zeit Agricultural Research Center.
CSA (2020). Agricultural sample survey 2019/20 (2012 E.C.). Report on Area and Production of Major Crops (Private Peasant Householdings, Meher Season). Central Statistics Authority of Ethiopia.
Dalal, A., Bourstein, R., Haish, N., Shenhar, I., Wallach, R. & Moshelion, M. (2019) Dynamic physiological phenotyping of drought-stressed pepper plants treated with “productivity-enhancing” and “survivability-enhancing” biostimulants. Frontiers in Plant Science, 10(905), 1-14.
Degu, H.D. (2010) Mapping QTLs related to plant height and root development of eragrostis tef under drought. Journal of Agricultural Science, 2(2), 62-72.
Degu, H.D., Ohta, M. & Fujimura, T. (2008) Drought tolerance of eragrostis tef and development of roots. International Journal of Plant Sciences, 169(6), 768-775.
Fàbregas, N. & Fernie, A.R. (2019) The metabolic response to drought. Journal of Experimental Botany, 70(4), 1077-1085.
Ferede, B., Mekbib, F., Assefa, K., Chanyalew, S., Abraha, E. & Tadele, Z. (2020) Evaluation of drought tolerance in tef [Eragrostis Tef (Zucc.) Trotter] genotypes using drought tolerance indices. Journal of Crop Science and Biotechnology, 23(2), 107-115.
Fisher, L.H., Han, J., Corke, F.M., Akinyemi, A., Didion, T., Nielsen, K.K. et al. (2016) Linking dynamic phenotyping with metabolite analysis to study natural variation in drought responses of brachypodium distachyon. Frontiers in Plant Science, 7, 1751.
Großkinsky, D.K., Svensgaard, J., Christensen, S. & Roitsch, T. (2015) Plant phenomics and the need for physiological phenotyping across scales to narrow the genotype-to-phenotype knowledge gap. Journal of Experimental Botany, 66(18), 5429-5440.
Guo, X., Xin, Z., Yang, T., Ma, X., Zhang, Y., Wang, Z. et al. (2020) Metabolomics response for drought stress tolerance in chinese wheat genotypes (Triticum aestivum). Plants (Basel, Switzerland), 9(4), 520.
Hayat, S., Hayat, Q., Alyemeni, M.N., Wani, A.S., Pichtel, J. & Ahmad, A. (2012) Role of proline under changing environments: a review. Plant Signaling & Behavior, 7(11), 1456-1466.
Jifar, H., Dagne, K., Tesfaye, K., Assefa, K. & Tadele, Z. (2020) Genetic diversity and population structure of tef [Eragrostis tef (Zucc.) Trotter] as revealed by SSR markers. Advances in Crop Science and Technology, 8(438), 1-9.
Kamies, R., Farrant, J.M., Tadele, Z., Cannarozzi, G. & Rafudeen, M.S. (2017) A proteomic approach to investigate the drought response in the orphan crop Eragrostis tef. Proteomes, 5(4), 32.
Kattupalli, D., Pinski, A., Sreekumar, S., Usha, A., Girija, A., Beckmann, M. et al. (2021) Non-targeted metabolite profiling reveals host metabolomic reprogramming during the interaction of black pepper with Phytophthora capsici. International Journal of Molecular Sciences, 22(21), 11433.
Kaur, H., Manna, M., Thakur, T., Gautam, V. & Salvi, P. (2021) Imperative role of sugar signaling and transport during drought stress responses in plants. Physiologia Plantarum, 171(4), 833-848.
Khan, M.I.R., Palakolanu, S.R., Chopra, P., Rajurkar, A.B., Gupta, R., Iqbal, N. et al. (2021) Improving drought tolerance in rice: ensuring food security through multi-dimensional approaches. Physiologia Plantarum, 172(2), 645-668.
Kim, S.L., Kim, N., Lee, H., Lee, E., Cheon, K.S., Kim, M. et al. (2020) High-throughput phenotyping platform for analyzing drought tolerance in rice. Planta, 252(3), 38.
Lenk, I., Fisher, L.H.C., Vickers, M. et al. (2019) Transcriptional and metabolomic analyses indicate that cell wall properties are associated with drought tolerance in Brachypodium distachyon. International Journal of Molecular Sciences, 20(7), 1758.
Li, B., Fan, R., Sun, G., Sun, T., Fan, Y., Bai, S. et al. (2021) Flavonoids improve drought tolerance of maize seedlings by regulating the homeostasis of reactive oxygen species. Plant and Soil, 461(1), 389-405.
Muanenda, S., Yabeker, A. & Ligani, S. (2019) Effect of environment on different traits of teff evaluated on Debrezeit research institution, Oromia, Ethiopia. International Journal of Scientific and Research Publications (IJSRP), 9(2), 8630. https://doi.org/10.29322/ijsrp.9.02.2019.p8630
Martinelli, F., Cannarozzi, G., Balan, B., Siegrist, F., Weichert, A., Blösch, R. et al. (2018) Identification of miRNAs linked with the drought response of tef [Eragrostis tef (Zucc.) Trotter]. Journal of Plant Physiology, 224-225, 163-172.
Mekuriaw, S., Tsunekawa, A., Ichinohe, T., Tegegne, F., Haregeweyn, N., Kobayashi, N. et al. (2020) Effect of feeding improved grass hays and eragrostis tef straw silage on milk yield, nitrogen utilization, and methane emission of lactating fogera dairy cows in Ethiopia. Animals, 10(6), 1021.
Mengistu, D.K. (2009) The influence of soil water deficit imposed during various developmental phases on physiological processes of tef (Eragrostis tef). Agriculture, Ecosystems & Environment, 132(3), 283-289.
Michaletti, A., Naghavi, M.R., Toorchi, M., Zolla, L. & Rinalducci, S. (2018) Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Scientific Reports, 8(1), 5710.
Naing, A.H. & Kim, C.K. (2021) Abiotic stress-induced anthocyanins in plants: their role in tolerance to abiotic stresses. Physiologia Plantarum, 172(3), 1711-1723.
Pang, Z., Chong, J., Zhou, G., De Lima Morais, D.A., Chang, L., Barrette, M. et al. (2021) MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Research, 49(W1), W388-W396.
Ravisankar, S., Abegaz, K. & Awika, J.M. (2018) Structural profile of soluble and bound phenolic compounds in teff (Eragrostis tef) reveals abundance of distinctly different flavones in white and brown varieties. Food Chemistry, 263, 265-274.
Riemann, M., Dhakarey, R., Hazman, M., Miro, B., Kohli, A. & Nick, P. (2015) Exploring jasmonates in the hormonal network of drought and salinity responses. Frontiers in Plant Science, 6. https://doi.org/10.3389/fpls.2015.01077
Salvi, P., Kamble, N.U. & Majee, M. (2020) Ectopic over-expression of ABA-responsive Chickpea galactinol synthase (CaGolS) gene results in improved tolerance to dehydration stress by modulating ROS scavenging. Environmental and Experimental Botany, 171, 103957.
Todaka, D., Shinozaki, K. & Yamaguchi-Shinozaki, K. (2015) Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Frontiers in Plant Science, 6. https://doi.org/10.3389/fpls.2015.00084
Tohge, T., Perez de Souza, L. & Fernie, A.R. (2018) On the natural diversity of phenylacylated-flavonoid and their in planta function under conditions of stress. Phytochemistry Reviews, 17(2), 279-290.
VanBuren, R., Man, W.C., Wang, X., Pardo, J., Yocca, A.E., Wang, H. et al. (2020) Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal tef. Nature Communications, 11(1), 884.
Yadav, B., Jogawat, A., Rahman, M.S. & Narayan, O.P. (2021) Secondary metabolites in the drought stress tolerance of crop plants: a review. Gene Reports, 23, 101040.
Yan, J., Aznar, A., Chalvin, C., Birdseye, D.S., Baidoo, E.E.K., Eudes, A. et al. (2018) Increased drought tolerance in plants engineered for low lignin and low xylan content. Biotechnology for Biofuels, 11(1), 195.
Živanović, B., Milić, K.S., Tosti, T., Vidović, M., Prokić, L. & Veljović Jovanović, S. (2020) Leaf soluble sugars and free amino acids as important components of abscisic acid-mediated drought response in tomato. Plants, 9(9), 1147.