Download Perspective Abiotic Stress Tolerance: From Gene Discovery in

Molecular Plant
•
Volume 2
•
Number 1
•
Pages 1–2
•
January 2009
PERSPECTIVE
Perspective
Abiotic Stress Tolerance: From Gene Discovery in
Model Organisms to Crop Improvement
Ray Bressana, Hans Bohnertb and Jian-Kang Zhuc,1
a Purdue University, Department of Horticulture and Landscape Architecture, 625 Agriculture Mall Drive, West Lafayette, IN 47907-2010, USA
b University of Illinois, Department of Plant Biology, ERML 196, 1201 W. Gregory Dr., Urbana, IL 61801, USA
c University of California, Botany and Plant Sciences, 2150 Batchelor Hall, Institute for Integrative Genome Biology, Riverside, CA 92521, USA
ABSTRACT Productive and sustainable agriculture necessitates growing plants in sub-optimal environments with less
input of precious resources such as fresh water. For a better understanding and rapid improvement of abiotic stress tolerance, it is important to link physiological and biochemical work to molecular studies in genetically tractable model
organisms. With the use of several technologies for the discovery of stress tolerance genes and their appropriate alleles,
transgenic approaches to improving stress tolerance in crops remarkably parallels breeding principles with a greatly expanded germplasm base and will succeed eventually.
Agriculture has provided the foundation for civilizations to begin and to prosper. In all societal endeavors, all progress relies
on stable, abundant food supplies that then provide time for
people to devote energies to other activities. Abundant food
production at specific geographical sites with climates suitable
for a year-round food supply allowed for the emergence, construction and proliferation of permanent communities of ever
more sophistication. Early communities were situated near reliable water sources with the consequence that crops became
gradually adapted/selected for growth under near optimal
conditions of water supply. Mesopotamia, literally the land
‘between rivers’, the lower reaches of the Indus in today’s
Pakistan, and the Yellow river (Huang He) in China are examples of cradles of these early civilizations.
These first farming communities based crop selection on
yield alone, partly because they were situated where wild sources of food (plant growth) were not dramatically challenged
by the environment, and this then is likely a major reason that
the germplasm bases of major crops are remarkably narrow,
and deficient in their genetic capacity for high yield under
highly variable environments. However, the importance of
the environment (especially the osmotic environment (mainly
quantity and quality of available water)) remains preeminent
and, today, with farmers facing competition for water from an
ever increasing array of industrial and urban users, water limitation has reached a stage at which armed conflict over water
can easily be envisioned.
As the human population still expands, it is already exceeding the capacity of productive areas with adequate water supply. In parts of the world, agriculture is performed on
unsuitable, marginal land. Notwithstanding these social and
political implications, the importance of the environment to
plant life is obvious. For example, coping with water loss,
selecting low-water requiring lines, and research on plant water relations have a long and extensive history. Not only in
early times, but even modern studies in the field of plant physiology have been replete with a focus on water relations and
related mineral nutrition. The plant physiologists’ toolbox, up
until recently, has been slow to include genetics, which is all
the more surprising because early studies had clearly indicated
that tolerance to unfavorable osmotic and other environmental conditions had a clear basis in genetic variation. However,
from these studies, it was concluded that stress tolerances, like
other complex traits such as yield, are strictly conferred, both
cumulatively and antagonistically, by many genes. This has
changed (Lippman and Tanksley, 2001).
Under careful examination, it can be seen that any trait
measured is really a quantitative trait and shows a continuous
distribution. It is only when the segregating germplasm is sufficiently different genetically that a clear separation of subpopulations can be made without sophisticated statistical
analyses. Or put another way, the germplasm often being studied contains insufficient variations at any of the many loci that
1
To whom correspondence should be addressed. E-mail jian-kang.zhu@
ucr.edu, fax 951-827-7115, tel. 951-827-7117.
ª The Author 2009. Published by the Molecular Plant Shanghai Editorial
Office in association with Oxford University Press on behalf of CSPP and
IPPE, SIBS, CAS.
doi: 10.1093/mp/ssn097
Received 10 December 2008; accepted 10 December 2008
2
|
Bressan et al.
d
Abiotic Stress Tolerance
control a trait and there appears to be no single locus for this
trait, and we then call it a quantitative trait. This situation has
prevailed over a long time (see Maggio et al., 2006).
Physiological, biochemical and genetic studies of environmental stress tolerance have also been slowed because of a lack
of consensus of how stress tolerance can be viewed as a measurable phenotype. Without a consensus phenotype(s), results
from different studies cannot be compared. The use of various
species for these studies also complicates the comparison of
results, as does studying of diverse developmental stages
and then drawing generalizations. What constitutes, for example, sensitivity to drought at an early developmental stage
in a plant’s life may not be a stressful condition at a later stage,
such as during seed filling. However, the extensive use of model
systems, especially Arabidopsis, has greatly reduced these problems. Thus, the exhaustive physiological work that has been able
to define the greatest degree of contribution to physiological
tolerance has finally begun to be linked to genetic differences.
We now understand that genetic variation for tolerance clearly
exists and can be organized into four major processes that
contribute to physiological tolerance: (1) water homeostasis,
(2) metabolic adjustment including hormone regulation, (3)
growth control, and (4) injury control (Zhu, 2002).
To identify the genes (genetic loci) that are involved in these
four major areas of osmotic tolerance physiology, there has
been intensive research effort for the last decade coincident
with the availability of the major molecular genetic tools introduced to the plant science community largely by the adoption of Arabidopsis as a versatile plant model system.
The earliest genetic approaches using this model plant and
its formidable tools were influenced greatly by the transcription control paradigm because transcription (TF) factors and,
subsequently, other signal components connected to TFs have
historical importance arising from the progress of understanding the gene to organism paradigm and also because specific
studies reporting that evolution in general and crop domestication, in particular, have apparently been influenced more
dramatically by mutations in TFs or mutations in gene promoters (controlled by TFs) than by mutations in other loci
(Doebley et al., 1997). We now understand through many genetic
studies that transcriptional control is very important to phenotype manifestation but that many other molecular components
and processes play important roles (see Maggio et al., 2003).
The future of crop improvement through genetic manipulations may be accomplished in three major phases. First, many
more loci involved in the trait of environmental adaptation
need to be identified. Models like Arabidopsis and rice and
their tolerant relatives will be essential for this process for
years to come. Second, the appropriate alleles for the major
(able to have qualitative effects) loci will need to be identified.
Wild relatives of each crop will be essential for this. Finally, the
exit of research from the lab to the field will be required using
qualitative alleles, sometimes with laboratory modification
(e.g. increased expression, altered time/space expression,
etc.). This will likely require various gene combinations,
probably reflecting more than one of the four physiological
processes.
This special issue of Molecular Plant, we believe, reflects
many of the aspects of this movement toward successful crop
improvement for stress tolerance (more accurately called
yield stability). Several reports, including those by Yang
et al., Agarwal et al., Chai et al., Fuji and Zhu, Kumar et al.,
Quist et al., Dong et al., and Ballachandra et al., advance
our knowledge of the four fundamental processes controlling
stress tolerance and, in many, indicate the participation of
new loci in these important processes.
The genetic components that control the injury response
have consistently been shown to be included in the growing
number of loci that can be characterized as major (qualitative)
loci. One report in this issue by Pitzchke et al. and Hu et al.
increases the realization of the importance of the injury system
and the signal networks supporting the injury response.
A number of reports in this issue provide novel and more detailed information concerning the involvement of hormone- and
light-mediated signaling in stress responses, including Gimeno
et al., Chai et al., Gimeno et al., Quist et al., Pitzchke et al., Hu
et al. and Wang et al. The number of works reported reflects
the high importance of hormone-mediated responses to the
environment. The report by Xiao et al. illustrates the rapid movement of plant stress biology to the greenhouse and field—a stage
that continues to be emphasized as more stress loci are identified
andcharacterized enoughto warrantthiscostlystep.Tworeviews
thatappearinthisissueemphasizebothalong-standingaspect of
plant stress biology, namely calcium/calmodulin-mediated signaling (Kim et al.), and a new under-utilized component, the
use of extremophile models by Anna Amtmann.
The overall impact of the articles in this issue should stimulate
many more researchers to utilize a genetic approach, especially
with models combined with a better understood connection of
the four complimenting areas of physiology and biochemistry to
the genetic component that controls them.
REFERENCES
Doebley, J., Stec, A., and Hubbard, L. (1997). The evolution of apical
dominance in maize. Nature. 386, 485–488.
Lippman, Z., and Tanksley, S.D. (2001). Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the
smallfruited wild species Lycopersicon pimpinellifolium and L.
esculentum var. giant heirloom. Genetics. 158, 413–422.
Maggio, A., Joly, R.J., Hasegawa, P.M., and Bressan, R.A. (2003). Can
the quest for drought tolerant crops avoid Arabidopsis any longer? In Crop Production Under Saline Environments: Global and
Integrative Perspectives, Goyal S.S., Sharma S.K., and Rains D.W.,
eds (Binghamton, NY: Food Products Press, The Howorth Press),
pp. 99–129.
Maggio, A., Zhu, J.-K., Hasegawa, P.M., and Bressan, R.A. (2006).
Osmogenetics: Aristotle to Arabidopsis. Plant Cell. 18,
1542–1557.
Zhu, J.-K. (2002). Salt and drought stress signal transduction in
plants. Annu. Rev. Plant Biol. 53, 247–273.