Molecular Studies of Abiotic Stress
Robert D. Hill
Plant Science Department

University of Manitoba
Winnipeg, MB R3T 2N2

Telephone: (204) 474-6087
FAX: (204) 474-7528


I am interested in molecular responses of plants to abiotic stress, i.e., stress associated with the physical environment. Current research is focused on hypoxic stress and abscisic acid (ABA), a plant hormone associated with a number of stress responses. hypoxic stress research began with the discovery that hemoglobins, normally associated with mammals, were ubiquitous in plants. These hemoglobins are unique in that they bind oxygen very tightly, resulting in their being oxygenated at very low oxygen concentrations. One of these hemoglobin genes was activated in plant tissues exposed to hypoxic conditions. In the course of our research to relate hemoglobin expression with metabolism during hypoxia, we found that nitric oxide (NO) production increased substantially in hypoxic plant tissue. The amount of measurable NO varied inversely with the hemoglobin levels in the hypoxic tissue. This lead us to experimentally establish the existence of a hemoglobin/NO cycle (see figure) in hypoxic plant tissue. The pathway cycles nitrate through nitrite, NO and back to nitrate with consumption of NAD(P). The NO to nitrate conversion uses oxygenated hemoglobin forming oxidized hemoglobin (methemoglobin), which is reduced back to hemoglobin by NAD(P)H. Since the redox state in the cell environment can become highly reductive during hypoxia, the cycle should result in the cell being having a higher oxidative state when the cycle is operative. This is observed experimentally in cells with varying expression of hemoglobin. Cells expressing hemoglobin during hypoxia maintain their energy status better than cells not expressing the gene. We think we have an explanation for this. We have found that root mitochondria can synthesize ATP under strictly anaerobic conditions using nitrite and NAD(P)H. NO is one of the products of the reaction. We believe that the hemoglobin serves two functions during this process: maintaining anaerobic conditions in the cell by its ability to scavenge oxygen at very low oxygen concentrations, and; reacting with NO, to remove a potentially toxic product, regenerating nitrate for the next round of the cycle. Our work continues to relate these events to other processes in the hypoxic cell.




Recent Publications

Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot 103: 259-268.

Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226: 465-474[pdf]

Igamberdiev AU, Baron KN, Hill RD (2007) Nitric Oxide as an Alternative Electron Carrier During Oxygen Deprivation. In L Lamattina, JC Polacco, eds, Nitric Oxide in Plant Growth, Development and Stress Physiology Vol 6. Springer Verlag, Berlin, pp 255-268 [pdf]

Dordas C, Hill RD (2006) Production of nitric oxide and reactions with plant hemoglobins under hypoxic stress. In Y Blume, D Durzan, P Smertenko, eds, Cell Biology and Instrumentation: UV Radiation, Nitric Oxide and Cell Death in Plants Vol 371. IOS Press, Amsterdam, pp 218-226

Igamberdiev AU, Stoimenova M, Seregélyes C, Hill RD (2006) Class-1 hemoglobin and antioxidant metabolism in alfalfa roots. Planta 233: 1041-1046 [pdf]

Igamberdiev AU, Bykova NV, Hill RD (2006) Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. Planta 233: 1033-1040 [pdf]

Nie X, Durnin DC, Igamberdiev AU, Hill RD (2006) Cytosolic calcium is involved in the regulation of barley hemoglobin gene expression. Planta 223: 542-549 [pdf]

Guy PA, Duff SMG, Nie X, Hill RD, Durnin D, Sowa A (2005) Nonsymbiotic plant hemoglobins to maintain cell energy status. US Patent No. 6936749

Igamberdiev AU, Baron K, Manac'h-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: Involvement in flooding stress and effects on hormone signalling. Ann Bot 96: 557-564  [pdf]

Manac'h-Little N., Igamberdiev AU, Hill RD (2005) Hemoglobin expression affects ethylene production in maize cell cultures. Plant Physiol Biochem 43: 485-489  [pdf]

Igamberdiev AU and Hill RD (2004) Nitrate, NO and hemoglobin in plant adaptation to hypoxia: An alternative to classic fermentation pathways. J Exp Bot 55: 2473-2483 [pdf]

Seregélyes C, Igamberdiev AU, Maassen A, Hennig A, Dudits D, Hill RD (2004) NO-degradation by alfalfa class 1 hemoglobin (Mhb1): a possible link to PR-1a gene expression in Mhb1-overproducing tobacco plants. FEBS Letters 571: 61-66 [pdf]

Igamberdiev AU, Bykova NV, Ens W, Hill RD (2004) Dihydrolipoamide dehydrogenase from porcine heart catalyzes NADH-dependent scavenging of nitric oxide. FEBS Letters 568: 146-150 [pdf]

Dordas C, Hasinoff BB, Rivoal J, Hill RD (2004) Class 1 hemoglobins, nitrate and NO levels in hypoxic maize cell suspension cultures. Planta 219: 66-72 [pdf]

Igamberdiev AU, Seregélyes C, Manac'h N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219: 95-102 [pdf]

Dordas C, Hasinoff BB, Igamberdiev AU, Manac’h N, Rivoal J, Hill RD (2003) Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant Journal 35: 763-770 [pdf]