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 Plant Phenomics: An Overview
1
Jitendra Kumar, Aditya Pratap, and Shiv Kumar

Abstract
Precise and accurate measurement of traits plays an important role in the
genetic improvement of crop plants. Therefore, a lot of development has
taken place in the area of phenomics in the recent past. Both forward and
reverse phenomics have been evolved, which can help in identification of
either the best genotype having the desirable traits or mechanism and
genes that make a genotype the best. This includes development of high
throughput non-invasive imaging technologies including colour imaging
for biomass, plant structure, phenology and leaf health (chlorosis, necro-
sis); near infrared imaging for measuring tissue and soil water contents;
far infrared imaging for canopy/leaf temperature; fluorescence imaging
for physiological state of photosynthetic machinery; and automated
weighing and watering for water usage imposing drought/salinity. These
phenomics tools and techniques are paving the way in harnessing the
potentiality of genomic resources in genetic improvement of crop plants.
These techniques have become much more advanced and have now
entered the era of high throughput integrated phenotyping platforms to
provide a solution to genomics-enabled improvement and address our
need of precise and efficient phenotyping of crop plants.

Keywords
Phenomics • Forward • Reverse • Phenome • Phenes • Genomics • Genes

1.1 Introduction
J. Kumar (*) • A. Pratap
Division of Crop Improvement, ICAR – Indian Institute Worldwide demand for crops is increasing rap-
of Pulses Research, Kalyanpur, Kanpur 208024,
idly due to rising global population, rising
Uttar Pradesh, India
e-mail: jitendra73@[Link] demand for biofuel and feed stocks and changing
food preferences. Meeting future demand of agri-
S. Kumar
International Centre for Agricultural Research in the Dry cultural production poses the greatest challenge
Areas, P.O. Box 6299, Rabat – Instituts, Rabat, Morocco to agricultural scientists and policy makers

J. Kumar et al. (eds.), Phenomics in Crop Plants: Trends, Options and Limitations, 1
DOI 10.1007/978-81-322-2226-2_1, # Springer India 2015
2 J. Kumar et al.

(Bruinsma 2003) because demand for cereals, phenotype in a ‘real world’ environment remains
biofuels and feed stocks has already surpassed elusive as many false positive QTL have been
the current supply and is expected to rise further reported earlier.
in the near future (Furbank et al. 2009; Sticklen Although a large collection of germplasm of
2007). Therefore, there is a competition among different crop species are available worldwide,
crops for arable land in order to increase their phenotypic descriptions of these genome wide
production. Rising global mean temperature by knockout collections are still limited. As a result,
0.8  C since the 1850s, which is expected to it restricted the use of genomic resources for
increase further by 1.8–4.0  C by the end of this identifying the allelic variation for a promising
century, will have further impact on agricultural candidate gene in natural germplasm collection
production due to changing climate (Solomon (see Miyao et al. 2007). The poor utilization of
et al. 2007) and prevalence of abiotic stresses genomic resources could also be due to the lack of
with more intensity and frequencies (Tester and analysis of invisible traits and sometimes com-
Langridge 2010). It has been estimated that in plex phenotypic effects of genetic modification.
future average crop yields may decline across Therefore, identification of a candidate germ-
Africa and South Asia by 8 % by the 2050s plasm that carries genes for targeted traits is
(Knox et al. 2012). These declines in yields only possible when we will have the precise and
have been predicted about 17 % in wheat, 5–16 accurate phenotyping profile of the germplasm.
% in maize, 11–15 % in sorghum, and 10 % in Phenotyping of valuable agricultural traits such
millet across above regions under regimes of as grain yield, abiotic stress tolerance, and
climate change (Wheeler and von Braun 2013). nutritional quality is widely recognized as the
Therefore, development of ‘climate-smart’ most laborious and technically challenging
germplasm would be a priority to tackle these because replicated trials are necessary across
future challenges of climate change (Ziska and multiple environments over a number of seasons.
Bunce 2007; Leakey et al. 2009). Some of the current phenotyping tools also
The use of conventional plant breeding require destructive harvesting at fixed time
methods has made substantial gain in crop yield intervals or at a particular phenological stage
worldwide. However, researchers are now and are slow and costly. These bottlenecks in
observing that current breeding methods will field phenotyping have driven intense interest
not be sufficient to meet the projected future over the past decade and hence efforts have
demand of foods (Furbank et al. 2009; Tester been made on development of new high through-
and Langridge 2010; Sticklen 2007). Therefore, put phenotyping tools and techniques such nonin-
this has shifted our focus towards the use of vasive imaging, spectroscopy, image analysis,
genomics and gene technology advances for robotics and high-performance computing for
assisting the current breeding programs in order phenotyping. These tools can not only be used
to increase grain yields. These developments are in laboratories but also in field leading to high-
being utilized in trait discovery, genetic dissec- throughput analysis of phenotypes in natural
tion of complex traits and discovery of associated conditions as well as under controlled-
genes and their deployment in varieties. This has environment conditions. Now, field evaluation
resulted so far in more than 5,000 publications on of plant performance is much faster, and
mapping of quantitative trait loci (QTL) and their facilitates a more dynamic, whole-of-lifecycle
isolation during the past years (Zamir 2013). In measurement less dependent on periodic destruc-
spite of these efforts, the identified QTLs/genes tive assays. The dedicated high throughput
could not be deployed in mainstream breeding controlled-environment facilities have also
programs because identification of most of these improved the precision in recording the data and
QTLs/genes was not based on the precise and reduce the need for replication in the field. Thus
accurate phenotyping data of targeted traits. these advances have revolutionized the field of
Hence, association of these QTL/genes with the the accurate and precise phenotyping for
1 Plant Phenomics: An Overview 3

important traits and bring us to the age of phenome is difficult due to the change in the
‘phenomics’ and overview of these developments phenotypic expression of traits over the environ-
have been presented in this chapter. mental conditions (Houle et al. 2010).

1.2 Origin of Plant Phenotyping 1.4 Phenotype vs Phenomics

Plant phenotyping has been a part of crop and Phenotype of a plant can be described on the
variety selection since the time of human civili- basis of morphological, biochemical, physiologi-
zation when humans selected the best individuals cal and molecular characteristics. Different
of a crop species for domestication (Diamond parameters are measured to describe these
1997). Subsequently it has become common characteristics. Johannsen (1911) has coined the
practice in plant breeding for selecting the best terms ‘genotype’ and ‘phenotype’. He
genotype after studying phenotypic expression in demonstrated substantial variation in quantita-
different environmental conditions and also tive traits to which he called ‘phenotypical’ in
using them in hybridization programs in order genetically-identical material and thus proved
to develop new improved genotypes (Pearson that variation in a given observed traits is not
et al. 2008; Fisher 1925; Annicchiarico 2002). controlled entirely by genetics. Therefore, use
Ecologists used phenotyping to study phenotypic of statistical analysis has been suggested for
plasticity of genotypes during the middle of the identifying the differences among genotypes
twentieth century and suggested the role of the because phenotypic variation within a genotype
genotype and environmental conditions in the can obscure phenotypic differences among
expression of plant phenotypes under which it genotypes. This leads to origin of pheno- word.
develops (Suzuki et al. 1981). Subsequently, After 1950, ‘phenotyping’ as a noun, ‘to pheno-
developments in ecology in relation to type’ as a verb and ‘phenome’ as the collective
phenotyping are the trait-based approaches, in noun were introduced, which have been accepted
which phenotypic characteristics of a wider scientifically and are being utilized commonly in
range of different species are evaluated either in literature.
the field (Reich et al. 1992) or under laboratory
conditions (Grime and Hunt 1975; Poorter et al.
1990). They were used to derive different 1.5 Forward and Reverse Plant
strategies by which the ecological niche of spe- Phenomics
cies could be described (Grime 1979) and to
analyze the interdependence of various traits Plant phenomics is the study of plant growth,
(Wright et al. 2004). performance and composition. Figure 1.1
showed the use of forward and reverse
phenomics in genetic improvement. Forward
1.3 Phenomics phenomics uses phenotyping tools to discrimi-
nate the useful germplasm having desirable traits
The word ‘phenome’ refers to the phenotype as a among a collection of germplasm. This leads to
whole (Soul 1967) i.e., expression of genome for identification of the ‘best of the best’ germplasm
a trait in a given environment while in phenomics line or plant variety. Use of high-throughput,
we get high-dimensional phenotypic data on an fully automated and low resolution followed by
organism at large scale. Actually phenomics is higher-resolution screening methods have
used as analogy to genomics. However it differs accelerated plant breeding cycle by screening a
from genomics. In genomics, complete charac- large number of plants at seedling stage. Thus
terization of a genome is possible while in interesting traits can be identified rapidly at early
phenomics, complete characterization of stage and there is no need to grow plants up to the
4 J. Kumar et al.

Fig. 1.1 Forward and reverse phenomics for genetic improvement in crop plants

maturity stage in field. Now it is possible in is not completely straight forward (Mahner and
forward phenomics to screen thousands of plants Kary 1997) and it varies among the various sub
in pots running along a conveyor belt, and disciplines of biology. Ecologists traditionally
travelling through a room containing automated define phenotype as trait when they refer to a
imaging systems such as infra-red or 3D phenotypic variable of a plant such as the specific
cameras. The pots are labelled with barcodes or leaf area (SLA). However, some ecologists also
radio tags, so that the system can identify which refer to traits in relation to characteristics of
pots contain plants with interesting traits. The vegetation, such as the leaf area index (LAI).
selected plants can then be grown up to produce Like gene, ‘trait’ has been designated as
seed for further analysis and breeding. ‘phene’. However it can be over simplification
The reverse phenomics is used where the best for a one-to-one relationship between gene and
of the best genotypes having desirable trait(s) is phene because one gene can have a range of
already known. Now through reverse phenomics, pleiotropic effects and many genes can control
traits shown to be of value to reveal mechanistic a trait. The term ‘phenome’ is being utilized as a
understanding are dissected in details and subse- counterpart to ‘genome’. Thus as total constella-
quently the identified mechanisms are exploited tion of all genes (alleles) present in an individual
in new approaches. Thus in reverse phenomics, is known as genome. Therefore, similarly the
we discover mechanisms which make ‘best’ phenome would be the aggregate of all the
varieties the best. This can involve reduction of expressed traits of an individual. Actually, use
a physiological trait to biochemical or biophysi- of various terminology may overlap as they ful-
cal processes and ultimately a gene or genes. For fill various and different needs for different
example, in case of drought tolerance, niches of the scientific community. A clear and
researchers try to work out the mechanisms singular definition throughout the full domain of
underlying the drought tolerance and find out biology is desirable but probably unreachable
the gene or genes that are responsible for (Mahner and Kary 1997).
it. These genes are screened in germplasm or
the gene can be bred into new varieties.
1.7 Advances in Phenomics

1.6 Genes and Phenes Morphological, physiological and biochemical

traits are important to breeders for making
To describe phenotype is more challenging than genetic improvement for yield, quality and toler-
genotype because it changes over the ance to biotic and abiotic stresses. These traits
environments. Therefore, the term ‘phenotype’ have been discussed in details in Chap. 2.
1 Plant Phenomics: An Overview 5

Conventionally, phenotyping data on these traits developed which is based on fluorescence param-
are recorded either visually or manually, which is eter measured in stress (Baker 2008). It can be
time-consuming and required a lot of efforts. used on whole leaves or small plants. It used
This also increases chance of errors in measure- successfully for abiotic stresses screening in
ment of traits. As a result, it increases chance to Arabidopsis and tobacco (Nicotiana tabacum)
identify the false positive alleles, which leads to or seedlings of dicots such as canola (Brassica
slow gain in genetic improvement. Therefore napus) or cotton (Gossypium ssp.) (Baker 2008;
during the past few years, focus has been shifted Woo et al. 2008). It can also be used to determine
on precise, accurate and rapid phenotyping of projected leaf area and hence the growth rate if
traits on a large scale. High-throughput measurements are taken regularly over time
phenotyping using non-invasive imaging (Barbagallo et al. 2003). The chlorophyll fluores-
technologies is a rapidly advancing field (www. cence images of the affected area of the leaf
[Link]; Furbank et al. 2009; allow the early detection of disease symptoms
Finkel 2009; Jansen et al. 2009; Berger et al. caused by the pathogens. These infected areas
2010). These techniques are based on colour can be quantified leading to identification of the
imaging for biomass, plant structure, phenology susceptible and resistant response to pathogen
and leaf health (chlorosis, necrosis), near infrared attack, at least in the case of mildew on barley
imaging for measuring tissue water content and leaves (Swarbrick et al. 2006; Chaerle et al.
soil water content, far infrared imaging for can- 2009). Leaf spectroscopy or hyperspectral reflec-
opy/leaf temperature, fluorescence imaging for tance spectroscopy using radiometric or, more
physiological state of photosynthetic machinery recently, imaging sensors are another established
and automated weighing and watering for water optical techniques related to chlorophyll fluores-
usage imposing drought/salinity conditions. cence, which have been developed to study the
These advanced phenotyping techniques have stress related phenomics (Jones and Vaughan
been discussed in details earlier in a number of 2010). However, its use in plant breeding is lim-
reviews (see Furbank and Teste 2011; Walter ited due to difficulties in interpreting canopy
et al. 2012). The genotypes capable of temperature data.
maintaining stomatal conductance under salt Digital imaging is one of the least compli-
induced osmotic stress have been selected suc- cated but useful methods for quantitatively deter-
cessfully at the young seedling stage in wheat mining the stress tolerance. It is popular
and barley using infrared thermography (Sirault approach for in situ crop phenotyping in con-
et al. 2009). This technique has also been trolled environment facilities. It uses to take the
suggested to use for high-throughput seedling digital images of growth over a period of plant
screening for drought tolerance in the vegetative development and measures quantitative changes
stages of crop development and has great poten- in images caused by the sum of stress response
tial for low-cost, high-throughput field mechanisms. In addition to this, taking digital
phenotyping. The genotypes having better pho- images in visible wavelength regions also give
tosynthetic capability and higher water use effi- opportunity to identify color of the plants. As a
ciency in field can be screened by measuring the result, it enables to quantify senescence arising
canopy temperature using handheld hermopile due to nutrient deficiencies or toxicities, or path-
based infrared thermometers (i.e. canopy temper- ogen infections. It has been used successfully to
ature ‘guns’). Chlorophyll fluorescence analysis quantify toxicity of germanium (as a toxic ana-
has been used to test the maintenance of photo- logue of boron) in a mapping population of bar-
synthetic function under biotic and abiotic ley (Schnurbusch et al. 2010) and identified a
stresses leading to identification of resistance QTL at the same locus as previously identified
and susceptible genotypes. For this purpose, a for boron tolerance using a visual score of
commercial instrument namely pulse amplitude- symptoms (Jefferies et al. 1999). The attempt
modulated (PAM) or fluorometry has been was also made to measure the water use
6 J. Kumar et al.

efficiency in plants (Harris et al. 2010). Use of and Tester 2011; Fiorani et al. 2012). In these
non-destructive imaging using fluorescence platforms, we can measure the plant size and leaf
and hyperspectral reflectance offers great prom- area of large germplasm collections using 2D
ise in quantitative scoring of such adult plant color images and dense canopy by using 3D
resistance phenotypes. However use these image technology and magnetic resonance imag-
techniques for screening biotic stresses is still ing (MRI) (Poorter et al. 1988; Dornbusch
limited. et al. 2012). The fluorescence and hyperspectral
analysis allow evaluation of various plant traits
in a fast and non-destructive manner to charac-
1.7.1 Development Towards the terize the leaves and roots at physiological or
Phenotyping Machines biochemical level. However, only specific
aspects of plant functioning can be evaluated in
ring the past one decade, vast amount of genomic this way. An exciting new development is the
resources have been developed and rapid devel- robotised sensor-actor for destructive sampling
opment in genome sequencing has increased the of relevant plant parts has widen the phenotyping
genomic data bases such as, e.g. GABI DB or capabilities by automated measurement of cellu-
TAIR DB in model plant species and crop plants lar processes and/or gene expression at specific
(Meinke et al. 1998; Riano-Pachon et al. 2009; time points (Alenyà et al. 2012). Relevance of a
Huala et al. 2001). High throughput genotyping laboratory and greenhouse phenotyping tech-
platforms have increased the speed of genotype nique is actually tested in field because traits
selection in breeding programs (Langridge and considered critical in the greenhouse may be
Fleury 2011). However phenotyping for complex less important in the field. For example, the can-
traits related to anatomy, morphology, physiol- opy of a stand is more relevant than of a single
ogy and development is still less advanced, plant under field conditions. Therefore, mobile
although high-throughput phenotyping platforms such as a tractor equipped with specific
techniques have increased our detection ability sensors enabled larger spatial flexibility have
substantially at subcellular level for protein been developed for the mechanistic field
interactions or metabolism (Houle 2010; phenotyping measurements with high accuracy
Kolukisaoglu and Thurow 2010). For plant and repeatability in given plots, while drones or
breeders, screening component traits airborne platforms can cover vast agricultural
contributing to yield under field conditions at areas. Though multi- and hyperspectral
large scale is more important for making genetic technologies (Rascher and Pieruschka 2008;
improvement, but it is still lacking (Furbank and Comar et al. 2012) can be used to analyze physi-
Tester 2011). However significant efforts have ological process, only few robust techniques such
been made towards the development of as the laser-induced fluorescence transient
automated phenotyping platforms during the (LIFT) approach are available to estimate photo-
past years (Granier et al. 2006; Jansen synthetic efficiency in the field (Pieruschka
et al. 2009; Furbank and Tester 2011; Delseny et al. 2010). Dedicated field sensors are already
et al. 2010; see Chap. 18) by taking advantages of applied in precision agriculture for nutrient man-
throughput phenotyping facilities developed in agement (Scotford and Miller 2005) and may
the field of drug discovery, development, and become important tools for sensing of plant dis-
animal behavior (Mayr and Bojanic 2009; ease in the near future (Mahlein et al. 2012).
Noldus et al. 2001). In brief, these platforms are Establishment of wireless sensor networks
equipped with sensor or image based systems enables continuous monitoring of the environ-
under the controlled growth leading to establish- ment and crop properties and will provide valu-
ment and implementation of the non-destructive able information for agricultural management
imaging approaches for phenotyping (Furbank (Ruiz-Garcia et al. 2009).
1 Plant Phenomics: An Overview 7

Fig. 1.2 Flow chart Identification of related traits

of application of
non-destructive yield, quality, tolerance to biotic and abiotic stresses
phenotyping in genetic etc.
dissection of trait Develop high throughput robust screening tools & techniques
color imaging, infrared thermography,
chlorophyll inflorescence etc.
Screening the genetic resources
genotypes having desirable traits.

Genetic dissection of individual traits

markers, gene sequences etc.

Validation and use of markers associated with trait to yield in the field

Phenomics has not only allowed to dissect the

1.8 Harnessing the Potentiality of complex traits through genomics but also helped
Genomics Through Phenomics to use genomic resources in discovering new
genes/QTL, identification of function of a gene
Vast amount of genomic resources are available sequence and helped to increase the genetic gain
in public domain but these could not be utilized for traits having low heritability (see chap. 17 for
with their potentially due to the lack of precise, details). This understanding will allow us to sim-
accurate and high throughput phenotyping tools ulate and predict plant properties in particular of
and techniques. Therefore, efforts have been complex traits such as yield or biomass, the most
made for the development of high throughput important challenge to address future needs of a
phenotyping tools and techniques for screening growing human population. Both forward and
of morpho-physiological traits related to biotic reverse phenomics approaches can be used to
and abiotic stresses. The genomic resources harness the potentiality of genomic resources.
developed in a plant species can be linked with The accurate, cost-effective, high-throughput
physiological and morphological data collected phenotyping is pivotal to fine mapping of traits,
using current phenotyping approaches available regardless of the genetic approach for producing
at automated phenotyping platforms worldwide. allelic recombination or assessing variation by
These high throughput phenotyping tools collect re-sequencing technologies. Phenomics can be
the precise and accurate observations and allow used in reverse genetic studies and can help to
analysis of data for understanding the whole identify the function of a particular gene(s) in
phenome of the plant under a wide range of growth and development of crop plants and can
environmental conditions. Thus like genomic be used to identify the allelic variation to target
platforms, phenotyping platforms develop the associated genes (Fig. 1.2).
databases such as the plant meta-phenomics data-
base (Poorter et al. 2010) or the Plant Trait data-
base TRY ([Link] accessed 1.9 Conclusion
September 2012) which bring together pheno-
typic responses to the environment for a wide For making successful genetic improvement in
range of plant traits and parameters. These crop plants, plant breeders first identify the desir-
phenotyping database along with available inter- able genotypes having target traits by screening a
national genomic databases (TAIR, TIGR and collection of germplasm accessions. These target
NCBI, and with other ‘omics’ information such traits then are combined together through
as metabolomic, proteomic and transcriptomic hybridization. This cycle of selection-
data) have now become important to understand hybridization-selection has been implementedon
the genetic architecture of complex traits. the basis of visual observation since
8 J. Kumar et al.

domestication of crop plants. Though visual perturbations of metabolism and plant growth using
screening is easy and precise for qualitative and chlorophyll fluorescence imaging. Plant Physiol
132:485–493, 37
highly heritable traits, its use is less precise for Berger B, Parent B, Tester M (2010) High throughput
quantitative traits and those traits, which are dif- shoot imaging to study drought responses. J Exp Bot
ficult to observe visually (physiological and bio- 61:3519–3528
chemical traits). Moreover, vast amount of Bruinsma J (2003) World agriculture: towards 2015/2030:
an FAO perspective. Earthscan, London
genomic resources have been developed in a Chaerle L, Lenk S, Leinonen I, Jones HG, Van Der
number of crop species in the past. The available Straeten D, Buschmann C (2009) Multi-sensor plant
gene sequences and molecular markers could still imaging: towards the development of a stress-
not be associated with any traits due to the lack of catalogue. Biotechnol J 4:1152–1167
Comar A, Burger PH, de Solan B, Baret F, Daumard F,
phenotyping of germplasm collections. For Hanocq JF (2012) A semi-automatic system for high
utilizing these genomic resources and identifica- throughput phenotyping wheat cultivars in-field
tion of desirable plants, the precise phenotyping conditions: description and first results. Funct Plant
of germplasm accessions for challenging traits is Biol 39:914–924
Delseny M, Han B, Hsing YI (2010) High throughput
required in various crop species. DNA sequencing: the new sequencing revolution.
In the recent past, various techniques and Plant Sci 179:407–422
methodologies have been developed for screening Diamond J (1997) Guns, germs, and steel: the fates of
biotic, abiotic, physiological and biochemical human societies. Norton and Company, New York
Dornbusch T, Lorrain S, Kuznetsov D, Fortier A,
traits in crop plants. These technologies have Liechti R, Xenarios I, Fiorani F, Rascher U, Jahnke
become very advanced in the era of digital sci- S, Schurr U (2012) Imaging plants dynamics in
ence. These plant phenomics developments are heterogenic environments. Curr Opin Biotechnol
actually helping to make simply plant physiology 23:227–235
Finkel E (2009) With ‘phenomics’ plant scientists hope to
in ‘new clothes’. Thus this trans-disciplinary shift breeding into overdrive. Science 325:380–381
approach promises significant new breakthroughs Fiorani F, Rascher U, Jahnke S, Schurr U (2012) Imaging
in plant science. Phenomics provides the opportu- plants dynamics in heterogenic environments. Curr
nity to study previously unexplored areas of plant Opin Biotechnol 23:227–235
Fisher RA (1925) Statistical methods for research
science, and it provides the opportunity to bring workers. Oliver & Boyd, Edinburgh
together genetics and physiology to reveal the Furbank RT, Tester M (2011) Phenomics – technologies
molecular genetic basis of a wide range of previ- to relieve the phenotyping bottleneck. Trends Plant
ously intractable plant processes. The challenges Sci 16:635–644
Furbank RT, von Caemmerer S, Sheehy J, Edwards G
ahead in plant-based agriculture will require the (2009) C4 rice: a challenge for plant phenomics. Funct
scale of quantum advances we have seen in infor- Plant Biol 36:845–856
mation technology in the past 20 years and we Granier C, Aguirrezabal L, Chenu K, Cookson SJ,
need to build on these advances for security of Dauzat M, Hamard P, Thioux JJ, Rolland G,
Bouchier-Combaud S, Lebaudy A, Muller B,
global food, fiber and fuel. Simonneau T, Tardieu F (2006) PHENOPSIS, an
automated platform for reproducible phenotyping of
plant responses to soil water deficit in Arabidopsis
thaliana permitted the identification of an accession
References with low sensitivity to soil water deficit. New Phytol
169:623–635
Alenyà G, Dellen B, Foix S, Torras C (2012) Leaf seg- Grime JP (1979) Plant strategies and vegetation pro-
mentation from time-of-flight data for robotized plant cesses. Wiley, Chichester
probing. IEEE Robot Autom Mag 20:50–59 Grime JP, Hunt R (1975) Relative growth rate: its range
Annicchiarico P (2002) Genotype  environment interac- and adaptive significance in a local flora. J Ecol
tion: challenges and opportunities for plant breeding 63:393–422
and cultivar recommendations. FAO Plant Production Harris BN, Sadras VO, Tester M (2010) A water-centred
and Protection Paper 74, FAO, Rome, pp 132 framework to assess the effects of salinity on the
Baker NR (2008) Chlorophyll fluorescence: a probe of growth and yield of wheat and barley. Plant Soil
photosynthesis in vivo. Annu Rev Plant Biol 336:377–389
59:89–113 Houle D (2010) Numbering the hairs on our heads: the
Barbagallo RP, Oxborough K, Pallett KE, Baker NR shared challenge and promise of phenomics. PNAS
(2003) ***Rapid, non-invasive screening for USA 107:1793–1799
1 Plant Phenomics: An Overview 9

Houle D, Govindaraju DR, Omholt S (2010) Phenomics: Noldus LPJJ, Spink AJ, Tegelenbosch RAJ (2001) Etho
the next challenge. Nat Rev Genet 11:855–866 vision: a versatile video tracking system for automa-
Huala E, Dickerman AW, Garcia-Hernandez M, tion of behavioral experiments. Behav Res Methods
Weems D, Reiser L, LaFond F, Hanley D, 3:398–414
Kiphart D, Zhuang M, Huang W, Mueller LA, Pearson CH, Ernst SM, Barbarick KA, Hatfield JL,
Bhattacharyya D, Bhaya D, Sobral BW, Beavis W, Peterson GA, Buxton DR (2008) Agronomy Journal
Meinke DW, Town CD, Somerville C, Rhee SY turns one hundred. Agron J 100:1–8
(2001) The Arabidopsis Information Resource Pieruschka R, Klimov D, Kolber Z, Berry JA (2010)
(TAIR): a comprehensive database and web-based Continuous measurements of the effects of cold stress
information retrieval, analysis, and visualization sys- on photochemical efficiency using laser induced fluo-
tem for a model plant. Nucleic Acids Res 29:102–105 rescence transient (LIFT) approach. Funct Plant Biol
Jansen M, Gilmer F, Biskup B, Nagel K, Rascher U, 37:395–402
Fischbach A, Briem S, Dreissen G, Tittmann S, Poorter H, Pot CS, Lambers H (1988) The effect of an
Braun S, De Jaeger I, Metzlaff M, Schurr U, elevated atmospheric CO2 concentration on growth,
Scharr H, Walter A (2009) Simultaneous phenotyping photosynthesis and respiration of Plantago major.
of leaf growth and chlorophyll fluorescence via Physiol Plant 73:553–559
GROWSCREEN FLUORO allows detection of stress Poorter H, Remkes C, Lambers H (1990) Carbon and
tolerance in Arabidopsis thaliana and other rosette nitrogen economy of 24 wild species differing in rela-
plants. Funct Plant Biol 36:902–914 tive growth rate. Plant Physiol 94:621–627
Jefferies SP, Barr AR, Karakousis A, Kretschmer JM, Poorter H, Niinemets U, € Walter A, Fiorani F, Schurr U
Manning S, Chalmers KJ, Nelson JC, Islam AKMR, (2010) A method to construct dose–response curves
Langridge P (1999) Mapping of chromosome regions for a wide range of environmental factors and plant
conferring boron toxicity tolerance in barley traits by means of a meta-analysis of phenotypic data.
(Hordeum vulgare L.). Theor Appl Genet J Exp Bot 61:2043–2055
98:1293–1303 Rascher U, Pieruschka R (2008) Spatio-temporal
Johannsen W (1911) The genotype conception of hered- variations of photosynthesis: the potential of optical
ity. Am Nat 45(531):129–159 remote sensing to better understand and scale light use
Jones HG, Vaughan RA (2010) Remote sensing of vege- efficiency and stresses of plant ecosystems. Precis
tation: principles, techniques and applications. Oxford Agric 9:355–366
University Press, Oxford Reich PB, Walters MB, Ellsworth DS (1992) Leaf
Knox J, Hess T, Daccache A, Wheeler T (2012) Climate life-span in relation to leaf, plant, and stand
change impacts on crop productivity in Africa and characteristics among diverse ecosystems. Ecol
South Asia. Environ Res Lett 7:034032 Monogr 62:365–392
Kolukisaoglu U, Thurow K (2010) Future and frontiers of Riano-Pachon DM, Nagel A, Neigenfind J, Wagner R,
automated screening in plant sciences. Plant Sci Basekow R, Weber E, Mueller-Roeber B, Diehl S,
178:476–484 Kersten B (2009) GabiPD: the GABI primary database
Langridge P, Fleury D (2011) Making the most of ‘omics’ – plant integrative ‘omics’ database. Nucleic Acids
for crop breeding. Trends Biotechnol 29:33–40 Res 37:D954–D959
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Ruiz-Garcia L, Lunadei L, Barreiro P, Robla JI (2009) A
Long SP, Ort DR (2009) Elevated CO2 effects on review of wireless sensor technologies and
plant carbon, nitrogen, relations: six important lessons applications in agriculture and food industry: state of
from FACE. J Exp Bot 60:2859–2876 the art and current trends. Sensors (Basel,
Mahlein AK, Oerke EC, Steiner U, Dehne HW (2012) Switzerland) 9:4728–4750
Recent advances in sensing plant diseases for preci- Schnurbusch T, Hayes JE, Sutton TJ (2010) Boron toxic-
sion crop protection. Eur J Plant Pathol 133:197–209 ity tolerance in wheat and barley: Australian
Mahner M, Kary M (1997) What exactly are genomes, perspectives. Breed Sci 60:297–304
genotypes and phenotypes? And what about Scotford IM, Miller PCH (2005) Applications of spectral
phenomes? J Theor Biol 186:55–63 reflectance techniques in northern European cereal
Mayr LM, Bojanic D (2009) Novel trends in high- production: a review. Biosyst Eng 90:235–250
throughput screening. Curr Opin Pharmacol Sirault XRR, James RA, Furbank RT (2009) A new
9:580–588. doi:10.1016/[Link].2009. 08.004 screening method for osmotic component of salinity
Meinke DW, Cherry JM, Dean C, Rounsley SD, tolerance in cereals using infrared thermography.
Koornneef M (1998) Arabidopsis thaliana: a model Funct Plant Biol 36:970–977
plant for genome analysis. Science 282:662–682 Solomon S, Qin D, Manning M, Chen Z, Marquis M,
Miyao A, Iwasaki Y, Kitano H, Itoh J, Maekawa M, Averyt KB, Tignor M, Miller HL (2007)
Murata K, Yatou O, Nagato Y, Hirochika H (2007) Climate change 2007: the physical science basis:
A large-scale collection of phenotypic data describing contribution of working group I to the fourth assess-
an insertional mutant population to facilitate func- ment report of the intergovernmental panel on
tional analysis of rice genes. Plant Mol Biol climate change. Cambridge Univ Press, New York,
63:625–635 pp 1–8
10 J. Kumar et al.

Soul M (1967) Phenetics of natural populations breeding of forage and turf species. Ann Bot
I. Phenetic relationships of insular populations of the 110:1271–1279
side-blotched lizard. Evolution 21:584–591 Woo N, Badger MR, Pogson BJ (2008) A rapid
Sticklen MB (2007) Feedstock crop genetic engineering non-invasive procedure for quantitative assessment
for alcohol fuels. Crop Sci 47:2238–2248 of drought survival using chlorophyll fluorescence.
Suzuki DT, Griffiths AJF, Lewontin RC (1981) An intro- Plant Methods 4:27
duction to genetic analysis, 2nd edn. W H Freeman, Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z,
New York Bongers F, Cavender-Bares J, Chapin T, Cornelissen
Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) The JHC, Diemer M, Flexas J, Garnier E, Groom PK,
metabolic consequences of susceptibility and the acti- Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W,
vation of race specific or broad spectrum resistance Lusk C, Midgley JJ, Navas ML, Niinemets U, €
pathways in barley leaves challenged with the pow- Oleksyn J, Osada N, Poorter H, Poot P, Prior L,
dery mildew fungus. Plant Cell Environ Pyankov VI, Roumet C, Thomas SC, Tjoelker MG,
29:1061–1076 Veneklaas EJ, Villar R (2004) The worldwide leaf
Tester M, Langridge P (2010) Breeding technologies to economics spectrum. Nature 428:821–827
increase crop production in a changing world. Science Zamir D (2013) Where Have All the Crop Phenotypes
327:818–822 Gone? PLoS Biol 11(6): e1001595. doi:10.1371/jour
Wheeler T, von Braun J (2013) Climate change impacts [Link].1001595
on global food security. Science 341:508–513 Ziska LH, Bunce JA (2007) Predicting the impact of
Walter A, Studer B, Kolliker R (2012) Advanced changing CO2 on crop yields: some thoughts on
phenotyping offers opportunities for improved food. New Phytol 175:607–618

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