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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Aerenchyma formation: programmed cell death in adventitious roots of winter wheat (Triticum aestivum) under waterlogging

Zhen Jiang A B , Xue-Fang Song A B , Zhu-Qing Zhou A C , Li-Kai Wang A , Ji-Wei Li A , Xiang-Yi Deng A and Hai-Yan Fan A
+ Author Affiliations
- Author Affiliations

A Laboratory of Cell Biology, College of Life Science and Technology, Huazhong Agricultural University, Wuhan, Hubei 430070, China.

B These authors contributed equally to this work.

C Corresponding author. Email: zhouzhuqing@mail.hzau.edu.cn

Functional Plant Biology 37(8) 748-755 https://doi.org/10.1071/FP09252
Submitted: 16 October 2009  Accepted: 29 March 2010   Published: 26 July 2010

Abstract

This study determined the characteristics of cortical cell death in wheat (Triticum aestivum L.) roots during programmed cell death (PCD) and the relationship between PCD and acid phosphatases. An examination of morphological development by light microscrope revealed that aerenchyma formed in roots waterlogged for 24 h and well developed aerenchyma formed in roots waterlogged for 120 h. The first detectable events were observed by electron microscopy and included plasma membrane invagination and the appearance of vesicles between the plasma membrane and the cell wall. Later, chromatin condensation and double-membrane-bound structures resembling autophagosomes were observed. The activity of acid phosphatases gradually increased during waterlogging and was present during the entire process of cell death. These observations suggest that cortical cell death during aerenchyma formation induced by waterlogging was a form of PCD. Acid phosphatases play an important role in PCD induced by waterlogging, being responsible for the hydrolysis of cell components at the later stages of PCD.

Additional keywords: acid phosphatases, adventitious roots, booting stage, PCD, TUNEL, ultrastructure.


Acknowledgements

This work was supported by the National Natural Foundation of China (Grant Nos 30571101). We thank JB Cao, GJ Shen, LJ Chai for technical assistance.


References


Aoyama H, Cavagis ADM, Taga EM, Ferreira CV (2001) Endogenous lectin as a possible regulator of the hydrolysis of physiological substrates by soybean seed acid phosphatase. Phytochemistry 58, 221–225.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bowen ID , Bowen SM (1990) Mechanisms of programmed cell death. In ‘Programmed cell death in tumors and tissues’. (Ed. ID Bowen) pp. 57–61. (Chapman & Hall: London)

Campbell R, Drew MC (1983) Electron microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage. Planta 157, 350–357.
Crossref | GoogleScholarGoogle Scholar | open url image1

Charvat I, Esau K (1975) An ultrastructural study of acid phosphatase localization in Phaseolus vulgaris xylem by the use of an azo-dye method. Journal of Cell Science 19, 543–561.
CAS |
open url image1

Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Functional Plant Biology 36, 665–681.
Crossref | GoogleScholarGoogle Scholar | open url image1

Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Molecular Biology Reporter 1, 19–21.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends in Plant Science 5, 123–127.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Evans DE (2004) Aerenchyma formation. New Phytologist 161, 35–49.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gahan PB (1978) A re-interpretation of the cytochemical evidence for acid phosphatase activity during cell death in xylem differentiation. Annals of Botany 42, 755–757.
CAS |
open url image1

Gahan PB, Maple AJ (1966) The behavior of lysosome-like particles during cell differentiation. Journal of Experimental Botany 17, 151–155.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gan XH, Ding YL (2006) The dynamic changes of acid phosphatase during the fiber development in Phyllostachys edulis culm. Journal of Nanjing Forestry University 30, 13–18. open url image1

Gladish DK, Xu JP, Niki T (2006) Apoptosis-like programmed cell death occurs in procambium and ground meristem of pea (Pisum sativum) root tips exposed to sudden flooding. Annals of Botany 97, 895–902.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Greenberg JT (1996) Programmed cell death: a way of life for plants. Proceedings of the National Academy of Sciences of the United States of America 93, 12 094–12 097.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Groover A, Dewitt N, Heidel A, Jones A (1997) Programmed cell death of plant tracheary elements: differentiation in vitro. Protoplasma 196, 197–211.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212, 205–214.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

He CJ, Morgan PW, Drew MC (1996) Transduction of an ethylene signal is required for cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiology 112, 463–472.
CAS | PubMed |
open url image1

Heryanto B, Yoshimura Y, Tamura T, Okamoto T (1997) Involvement of apoptosis and lysosomal hydrolase activity in the oviducal regression during induced molting in chickens: a cytochemical study for end labelling of fragmented DNA and acid phosphatase. Poultry Science 76, 67–72.
CAS | PubMed |
open url image1

Huang B, Johnson JW, Nesmith S, Bridges DC (1994) Growth, physiological and anatomical responses of two wheat genotypes to waterlogging and nutrient supply. Journal of Experimental Botany 45, 193–202.
Crossref | GoogleScholarGoogle Scholar | open url image1

Huang B, Johnson JW, Box JE, Nesmith DS (1997) Root characteristics and hormone activity of wheat in response to hypoxia and ethylene. Crop Science 37, 812–818.
CAS |
open url image1

Ibrahim H, Pertl H, Pittertschatscher K, Fall-Allah E, El-Shahed A, Bentrup FW, Obermeyer G (2002) Release of an acid phosphatase activity during lily pollen tube growth involves components of the secretory pathway. Protoplasma 219, 176–183.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1, 274–287.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Lenochová Z, Soukup A, Votrubová O (2009) Aerenchyma formation in maize roots. Biologia Plantarum 53, 263–270.
Crossref | GoogleScholarGoogle Scholar | open url image1

Li JC, Dong Q, Yu SL (2001) Effects of waterlogging at different growth stages on photosynthesis and yield of different wheat cultivars. Acta Agronomica Sinica 27, 434–441. open url image1

Lin J, Uwate WJ, Stallman V (1977) Ultrastructural localization of acid phosphatase in the pollen tube of Prunus avium L. (sweet cherry). Planta 135, 183–190.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Luigi B, Papini A, Milocani E, Vesprini JL (2006) Programmed cell death in the nucellus of Tillandsia (Bromeliaceae). Caryologia 59, 334–339. open url image1

Malik AI, Colmer TD, Lambers H, Schortemeyer M (2003) Aerenchyma formation and radial O2 loss along adventitious roots of wheat with only the apical root portion exposed to O2 deficiency. Plant, Cell & Environment 26, 1713–1722.
Crossref | GoogleScholarGoogle Scholar | open url image1

Niki T, Gladish DK (2001) Changes in growth and structure of pea primary roots (Pisum sativum L. cv. Alaska). Plant & Cell Physiology 42, 694–702.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Russell SW, Rosenau W, Lee JC (1972) Cytolysis induced by human lymphotoxin: cinemicrographic and electron microscopic observations. American Journal of Pathology 69, 103–118.
CAS | PubMed |
open url image1

Saab IN, Sachs MM (1996) A flooding-induced xyloglucan endotransglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiology 112, 385–391.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Saqib M, Akhtar J, Qureshi RH (2005) Na+ exclusion (Triticum aestivum) in saline-waterlogged conditions are improved by the development of adventitious nodal roots and cortical root aerenchyma. Plant Science 169, 125–130.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Schussler EE, Longstreth DJ (1996) Aerenchyma develops by cell lysis in roots and cell separation in leaf petioles in Sagittaria lancifolia (Alismataceae). American Journal of Botany 83, 1266–1273.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schussler EE, Longstreth DJ (2000) Changes in cell structure during the formation of root aerenchyma in Sagittaria lancifolia (Alismataceae). American Journal of Botany 87, 12–19.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Seago JLJR, Marsh LC, Stevens KJ, Soukup A, Votrubova O, Enstone DE (2005) A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Annals of Botany 96, 565–579.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thomson CJ, Colmer TD, Watkin ELJ, Greenway H (1992) Tolerance of wheat (Triticum aestivum cvs Gamenya and Kite) and triticale (Triticosecale cv. Muir) to waterlogging. New Phytologist 120, 335–344.
Crossref | GoogleScholarGoogle Scholar | open url image1

Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytologist 170, 213–226.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wang YQ, Chai JJ, Cui KM (1999) Ultracytochemical localization of acid phosphatase during differentiation and dedifferentiation of the secondary xylem in Eucommia ulmoides trunk. Acta Botanica Sinica 41, 1155–1159.
CAS |
open url image1

Wang LK, Zhou ZQ, Song XF, Li JW, Deng XY, Mei FZ (2008) Evidence of ceased programmed cell death in metaphloem sieve elements in the developing caryopsis of Triticum aestivum L. Protoplasma 234, 87–96.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Watkin ELJ, Thomson CJ, Greenway H (1998) Root development and aerenchyma formation in two wheat cultivars and one triticale cultivar grown in stagnant agar and aerated nutrient solution. Annals of Botany 81, 349–354.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wodzicki TJ, Brown CL (1973) Organization and breakdown of the protoplast during maturation of pine tracheries. American Journal of Botany 60, 631–640.
Crossref | GoogleScholarGoogle Scholar | open url image1

Wyllie AH, Morris RG, Smith AL, Dunlop D (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. The Journal of Pathology 142, 67–77.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Xiong H, Li YS, Li LJ (2006) A unique form of cell death occurring in meristematic root tips of completely submerged maize seedlings. Plant Science 171, 624–631.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zhou ZQ, Wang LK, Li JW, Song XF, Yang CN (2009) Study on programmed cell death and dynamic changes of starch accumulation in pericarp cells of Triticum aestivum L. Protoplasma 236, 49–58.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1