Aerenchyma and barrier to radial oxygen loss are formed in roots of Taro (Colocasia esculenta) propagules under flooded conditions

Abstract

Taro (Colocasia esculenta (L.) Schott) is cultivated primarily for its starchy underground stem (i.e., corm). It is adapted to both upland and wetland (i.e., flooded) conditions. Although taro is exposed to hypoxia that occurs in waterlogged soil, the mechanisms of its adaptation to hypoxia were unknown. To clarify the below-ground adaptation of taro to wetland conditions, we grew five taro cultivars/landraces hydroponically for 8 days under hypoxic conditions (n = 3) and analyzed: (1) the length of the longest root that emerged from the vegetative propagule; (2) aerenchyma (i.e., tissues containing air spaces); and (3) oxidation conditions around sides of root tips. Wild taro Āweu and the Chinese cultivar Bun-long had significantly longer roots than the Hawaiian cultivars/landraces Maui Lehua, Pi‘i‘ali‘i, and Ele‘ele Naioea (P < 0.05). Formation of aerenchyma, or air spaces that allow effective transportation of oxygen under hypoxic conditions, was observed consistently in roots of Āweu and Bun-long, but only occasionally in those of Hawaiian cultivars/landraces. In all cultivars/landraces, a pattern of radial oxygen leakage was detected only near root tips. In summary, taro appears to form aerenchyma and oxidize the rhizosphere around root tips under wetland conditions.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

ROL barrier:

Barrier to radial oxygen loss

References

  1. Abiko T, Obara M (2014) Enhancement of porosity and aerenchyma formation in nitrogen-deficient rice roots. Plant Sci 215–216:76–83

    Article  Google Scholar 

  2. Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant, Cell Environ 35:1618–1630

    CAS  Article  Google Scholar 

  3. Arikado H, Ikeda K, Taniyama T (1990) Anatomico–ecological studies on the aerenchyma and the ventilating system in rice plants. Bull Fac Bioresour Mie Univ 3:1–24

    Google Scholar 

  4. Armstrong W (1971) Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiol Plant 25:192-197

    Article  Google Scholar 

  5. Armstrong J, Armstrong W (1988) Phragmites australis—a preliminary study of soil-oxidizing sites and internal gas transport pathways. New Phytol 108:373–382

    Article  Google Scholar 

  6. Armstrong W, Armstrong J (2014) Plant internal oxygen transport (diffusion and convection) and measuring and modelling oxygen gradients. Low-oxygen stress in plants. Springer, Heidelberg, p 267-197

    Google Scholar 

  7. Colmer TD (2003a) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell Environ 26:17–36

    CAS  Article  Google Scholar 

  8. Colmer TD (2003b) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309

    CAS  Article  Google Scholar 

  9. Colmer TD, Gibbered MR, Wiengweera A, Tinh TK (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. J Exp Bot 49:1431–1436

    CAS  Article  Google Scholar 

  10. Evans D (2008) TARO Mauka to Makai. College of tropical agriculture and Human Resource of Hawai’i

  11. Ikezawa K (2015) Study on flooded cultivation of taro (Colocasia esculenta (L.) Schott)). Dissertation, Kagoshima University

  12. Ikezawa K, Fukumoto S, Onjo M, Yoshida R, Iwai S (2014) Effects of flooding on growth and yield of Taro (Clocasia esculenta Schott cv. ‘Daikichi’) in pot culture. Hort Res (Japan) 13:35–40

    Article  Google Scholar 

  13. Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495

    Article  Google Scholar 

  14. Kawai M, Samarajeewa PK, Barrero RA, Nishiguchi M, Uchimiya H (1998) Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 204:277–287

    CAS  Article  Google Scholar 

  15. Konishi T (2013) Taro imo ha kataru. Tokyo University of Agriculture

  16. Kotula L, Steudle E (2009) Measurements of oxygen permeability coefficients of rice (Oryza sativa L.) roots using a new perfusion technique. J Exp Bot 60:567–580

    CAS  Article  Google Scholar 

  17. Mae T, Ohira K (1981) The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol 22:1067–1074

    CAS  Google Scholar 

  18. Malik AI, Islam AK, Colmer TD (2011) Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum-wheat amphiploids. New Phytol 190:499–508

    CAS  Article  Google Scholar 

  19. Mano Y, Muraki M, Takamizo T (2006) Identification of QTL controlling flooding tolerance in reducing soil conditions in maize (Zea mays L.) seedlings. Plant Prod Sci 9:176–181

    CAS  Article  Google Scholar 

  20. Nakao S (1966) The origin of farming and cultivated plants, blue edn. Tokyo, Iwanami Shoten, p 103

    Google Scholar 

  21. Osorio NW, Shuai X, Miyasaka S, Wang B, Shirey RL, Wigmore WJ (2003) Nitrogen level and form affect taro growth and nutrition. Hort Sci 38:36–40

    Article  Google Scholar 

  22. Ponnamperuma FN (1984) Effects of flooding on soils. In: Kozlowski TT (ed) Flooding and plant growth. Academic Press, Orlando, pp 9–45

    Chapter  Google Scholar 

  23. Pujol V, Wissuwa M (2018) Contrasting development of lysigenous aerenchyma in two rice genotypes under phosphorus deficiency. BMC Res Notes 11:60

    Article  Google Scholar 

  24. Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat barley and oats. Plant Soil 253:1–34

    CAS  Article  Google Scholar 

  25. Shiono K (2016) A barrier to radial oxygen loss enables wetland plants to grow under waterlogged condition. Root Res 25:47–62

    Article  Google Scholar 

  26. Shiono K, Ogawa S, Yamazaki S, Isoda H, Fujimura T, Nakazono M, Colmer TD (2011) Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann Bot 107:89–99

    CAS  Article  Google Scholar 

  27. Stein BD, Strauss MS, Scheirer DC (1983) Anatomy and histochemistry of Taro, Colocasia esculenta (L.) Schott, leaves. International Society for Tropical Root Crops, 6th International Triennial Symposium of the International Society for Tropical Root Crops

  28. Suematsu K, Abiko T, Nguyen VL, Mochizuki T (2017) Phenotypic variation in root development of 162 soybean accessions under hypoxia condition at the seedling stage. Plant Prod Sci 20:323–335

    Article  Google Scholar 

  29. Takai Y (1978) Process of oxidation and reduction of waterlogged soil. Suiden dojogaku. Kodansha Inc., Tokyo

    Google Scholar 

  30. Whitney LD, Bowers FAI, Takahashi M (1939) Taro varieties in Hawaii. Hawaii agricultural experiment station of the University of Hawaii, Bulletin No. 84

Download references

Acknowledgment

The authors thank Ms. Sharon Wages (Assistant Extension Agent, University of Hawaii), Mr. Jedidiah Akao (UH student assistant), and Mr. Osamu Jahana for assistance with experiments. Also, we thank Mr. Christopher Bernabe (UH Agricultural Research Technician) for stimulating discussions about taro. Finally, we thank Dr. Hiroki Sakagami and Prof. Toshihiro Mochizuki of Kyushu University for their kind support. This work was supported by Support project for young teacher at the Graduate School of Agriculture, Kyushu University.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tomomi Abiko.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 246 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abiko, T., Miyasaka, S.C. Aerenchyma and barrier to radial oxygen loss are formed in roots of Taro (Colocasia esculenta) propagules under flooded conditions. J Plant Res 133, 49–56 (2020). https://doi.org/10.1007/s10265-019-01150-6

Download citation

Keywords

  • Taro
  • Wetlands
  • Rhizosphere
  • Aerenchyma
  • Oxidation
  • Roots